Dissecting the paleocontinental and paleoenvironmental dynamicsof the great Ordovician biodiversification

Franziska Franeck and Lee Hsiang Liow

Abstract.—The Ordovician was a time of drastic biological and geological change. Previous work hassuggested that there was a dramatic increase in global diversity during this time, but also has indicatedthat regional dynamics and dynamics in specific environments might have been different. Here, wecontrast two paleocontinents that have different geological histories through the Ordovician, namelyLaurentia and Baltica. The first was situated close to the equator throughout the whole Ordovician,while the latter has traversed tens of latitudes during the same time. We predict that Baltica, which wasunder long-term environmental change, would show greater average and interval-to-interval originationand extinction rates than Laurentia. In addition, we are interested in the role of the environment in whichtaxa originated, specifically, the patterns of onshore–offshore dynamics of diversification, where onshoreand offshore areas represent high-energy and low-energy environments, respectively. Here, we predictthat high-energy environments might be more conducive for originations.

Our new analyses show that the global Ordovician spike in genus richness from the Dapingian to theDarriwilian Stage resulted from a very high origination rate at the Dapingian/Darriwilian boundary,while the extinction rate remained low. We found substantial interval-to-interval variation in the origin-ation and extinction rates in Baltica and Laurentia, but the probabilities of origination and extinction aresomewhat higher in Baltica than Laurentia. Onshore and offshore areas have largely indistinguishableorigination and extinction rates, in contradiction to our predictions. The global spike in originationrates at the Dapingian/Darriwilian boundary is apparent in Baltica, Laurentia, and onshore and offshoreareas, and abundant variability in diversification rates is apparent over other time intervals for thesepaleocontinents and paleoenvironments. This observation hints at global mechanisms for the spike inorigination rates at the Dapingian/Darriwilian boundary but a domination of more regional and localmechanisms over other time intervals in the Ordovician.

Franziska Franeck. Natural History Museum, University of Oslo, Post Office Box 1172, Blindern, N-0318, Oslo,Norway. E-mail: franziska.franeck@nhm.uio.no

Lee Hsiang Liow. Natural History Museum, University of Oslo, Post Office Box 1172, Blindern, N-0318, Oslo,Norway; Centre for Ecological and Evolutionary Synthesis, Department of Biosciences, University of Oslo, PostOffice Box 1066, Blindern, N-0316, Oslo, Norway. E-mail: l.h.liow@ibv.uio.no

Accepted: 21 January 2019Data available from the Dryad Digital Repository: https://doi.org/10.5061/dryad.nk218ht

Introduction

The numerical increase of marine orders,families, and genera in the Ordovician was sodramatic (Sepkoski et al. 1981; Miller 1997a,b,2012; Sepkoski 1997; Harper 2006; Bassettet al. 2007; Alroy et al. 2008) that it has beentermed the great Ordovician biodiversificationevent (GOBE; Webby et al. 2004; Servais andHarper 2018). This increase is thought to beespecially rapid around the Dapingian/Darri-wilian boundary (Servais et al. 2009; Hintset al. 2010; Rasmussen et al. 2016; Trubovitzand Stigall 2016), but factors influencing thisincrease remain obscure.While the hypotheses for what these factors

might be are many and varied, it is possibleto group them into two classes. The first class

of hypotheses is climate related. Specifically, amid-Ordovician cooling is thought to have con-tributed to a more favorable global climateregime that in turn promoted diversification(Trotter et al. 2008; Rasmussen et al. 2016).The second class of hypotheses involves nutri-ent availability. For instance, periods ofincreased tectonics (Miller and Mao 1995)and/or tectonically induced volcanic activity(Botting 2002) are hypothesized to have led tomore sedimentary and nutritional input intothe oceans and habitat fractioning, both ofwhich may have enhanced the diversificationof taxa (Miller and Mao 1995). The establish-ment of nutrient-rich upwelling zones hasbeen documented from Laurentia during theMiddle Ordovician (Pope and Steffen 2003).

Paleobiology, 0(0), 2019, pp. 1–14DOI: 10.1017/pab.2019.4

© 2019 The Paleontological Society. All rights reserved. This is an Open Access article, distributed under the terms of theCreative Commons Attribution licence (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted re-use, distribution, and reproduction in any medium, provided the original work is properly cited. 0094-8373/19

These upwelling zonesmay have served as newecospace (Rasmussen et al. 2016), and their sub-sequent occupation by both migrants and taxathat evolved in situ could have contributed toan increase in taxon diversity. Some of themechanisms that were suggested to have aninfluence on the GOBE, such as tectonic activityand volcanism, likely acted at a regional ratherthan the global scale, and such regionalchanges are unlikely to be simultaneous (Miller1997a,b, 2004; Zhan and Harper 2006). There-fore the influence of the different mechanismsshould be examined separately for the differentpaleocontinents (Miller 1997a; Miller and Mao1998) and paleoenvironments (e.g., Miller andMao 1995; Miller and Connolly 2001; Novack-Gottshall and Miller 2003).Continents drifted and experienced different

spatial environments over the Ordovician.Whereas the center of the paleocontinent Laur-entia was situated close to the equator through-out the Ordovician, Baltica rotated northward,starting in the southern mid-latitudes and end-ing south of the equator by the Late Ordovician(Cocks and Torsvik 2006; Torsvik and Cocks2016a). These two continents can act as modelsystems for a relatively stable continent (Laur-entia) versus a continent on which the physicalenvironmental is relatively unstable due to con-tinental movement (Baltica) during the time inquestion. In this paper, we explore whethergreater environmental change on Baltica isassociated with greater taxon turnover butlower genus richness comparedwith Laurentia.Different paleoenvironments may also influ-

ence diversification rates. For instance, mor-phological novelties, as represented byordinal-level originations, arose preferentiallyin onshore rather than offshore areas (Jablonskiet al. 1983; Jablonski 2005). Based on his workon ordinal-level originations, Jablonski(Jablonski et al. 1983; Jablonski 2005) predictedthat genus originations would preferentiallyoccur where their higher-level taxa werealready established. If this is true, we expectthat relative origination dynamics might besimilar for onshore and offshore areas, allthings being otherwise equal. However, off-shore areas are more shielded from environ-mental changes than onshore areas, wherechanges in sea levels lead to changes in the

size of habitable areas (Holland and Christie2013). Here, we explore whether greater envir-onmental variability in onshore areas is asso-ciated with higher genus origination andextinction rates compared with offshore areasduring the Ordovician.We present Ordovician genus origination

and extinction rates based on capture–recap-ture models for the revised global Ordovicianstages (Bergström et al. 2009; Harper and Ser-vais 2013; Lindskog et al. 2017) both on a globalscale, for the paleocontinents Baltica and Laur-entia, and for onshore and offshore areas.

Methods and Data

Data.—We downloaded data from the Paleo-biology Database (PBDB) on 26 January 2018(https://paleobiodb.org/data1.2/occs/list.csv?taxon_reso=genus&interval=Cambrian,Aeronian&show=class,acconly,ecospace,coll,coords,loc,paleoloc,lithext,geo,refattr). These data consistof 130,367 occurrences of taxa identified to atleast the genus level that span the Cambrian tothe Aeronian (second stage in the Silurian) andtheir metadata. Only accepted genus nameswere included in our data analyses (73,735occurrences). Although our analyses are focusedon the Ordovician, we included Cambrian andSilurian data to ameliorate edge effects (see sub-section on diversification rates).The temporal resolution associated with the

data we retained from the PBDB downloadrange from 0.4 to 66.2 Myr. Considering onlyOrdovician time intervals, the resolution isfrom 1.7 to 50.8 Myr (median: 7.8 Myr; mean:8.6 Myr). To increase the temporal resolutionof our analyses, we only included PBDB datathat were assigned to time bins smaller than12 Myr (see Supplementary Material text andSupplementary Fig. S1). For occurrencesreported in PBDB with regional Ordovicianstages, we randomly assigned point estimatesusing a uniform distribution between thereported minimum and maximum ages andthen assigned those estimates to global Ordovi-cian stages (median: 7.7 Myr; mean: 5.9 Myr).This was to ensure comparability to standard,global treatments of Ordovician data. We pre-sent only one iteration of parameter estimatesin our main figures. But because random

FRANZISKA FRANECK AND LEE HSIANG LIOW2

assignments to time intervals vary, we also pre-sent averaged parameter estimates from 100iterations of such random assignments to theglobal data set or subsets for each of our ana-lyses in the Supplementary Material.We created a non-observation/observation

matrix from the downloaded PBDB data. Inthis matrix, each row of data is a string of obser-vations (1) or non-observations (0) of a genuswithin sequential global stages. We estimatedextinction, origination, and sampling rates byapplying a capture–recapture modeling frame-work to these data. Although there are manydifferent models within the capture–recapturemodeling framework (Nichols and Pollock1983; Liow and Nichols 2010), we follow previ-ous paleontological applications (Connolly andMiller 2001b; Liow et al. 2015; Kröger 2017) inusing the Pradel seniority model (Pradel 1996)for estimating diversification rates. In addition,we use the POPAN model (Schwarz andArnason 1996) for estimating genus richness.We note that up to 65% of our global genus

data set is made up of arthropods, brachiopods,and mollusks. The remaining 35% of thephyla in the data set are bryozoans, chordates,cnidarians, echinoderms, hemichordates, andporiferans.

Diversification Rates.—The Pradel senioritymodel (Pradel 1996) was developed for estimat-ing population parameters, namely survivalprobability w, seniority probability γ, samplingprobability p, and population growth λ.Because our data represent genera rather thanindividuals, these parameters reflect, respect-ively, genus survival probability (the comple-ment of which is genus extinctionprobability), genus “seniority” probability (thecomplement of which is genus originationprobability), sampling probability, and diversi-fication rates. Very briefly, we assume that gen-era are sampled within time intervals, i. Wenumber these from older (i) to younger geo-logical intervals (i + 1). In this framework, sur-vival (w) is the probability that a genus that isextant in a given time interval continues to beextant in the next time interval. Extinctionprobability (1− w) is hence the probability of agenus going extinct in the next time interval,given that it was extant in the time interval inquestion. Similarly, seniority probability γ

describes the probability that if a genus wasextant in time i + 1, it was already extant intime i. In this case, 1− γ is the origination prob-ability between the two time intervals. Diversi-fication λ describes howmuch a group of taxa isgrowing or declining from one time interval tothe next, where the net diversification rate is λi− 1. If the number of genera increases from onetime interval (i) to the next (i + 1), the net diver-sification ratewill be positive, while if the num-ber of genera is decreasing, it will be negative.A value of zero indicates no net increase ordecrease in the number of genera. Given thatthe Pradel seniority model has been previouslydetailed for paleontological data sets (Connollyand Miller 2001a,b, 2002; Liow and Nichols2010; Liow et al. 2015), we refer readers tothose publications for further details. It is suffi-cient to note that a logit link is used and that theparameters are estimated in a maximum-likelihood framework.As already mentioned, the basic parameters

of the Pradel seniority model are survival, seni-ority, and sampling probabilities. These basicparameters can be specified in different ways.For example, we can assume that they are con-stant through time (time-constant model).Using origination probability as an example,this means that time interval i has the same ori-gination probability as time interval i + 1, andso on, such that there is only one estimate forthe whole of the Ordovician. Because eventprobabilities increase as the sampling intervalsincrease, we specify wt or γt, with t being theduration between two sampling occasionssuch that origination and extinction probabil-ities can be interpreted in this time-constantmodel. Another model we could use is a fullytime-varying one, meaning that estimates(e.g., for origination) are allowed to be differentfor every time interval. Here, to allow compar-isons of our estimates across these stages, wetransform the estimated probabilities intorates by using a Poisson model. Specifically,Φi =−log[1−(1−w)i]/Ti for the extinction rateΦi, Γi =−log[1−(1−γ)i]/Ti for the originationrate Γi, and Pi =−log[1− (1− p)i]/Ti for thesampling rate Pi (Liow et al. 2015), with Ti

being the duration of one time interval. Add-itionally, we can add covariates to the model,such as affiliation with Laurentia or Baltica, in

DIVERSIFICATION DYNAMICS OF THE GOBE 3

order to estimate separate parameters for thetwo groups simultaneously. We specified andexaminedmanymodels (see “Results”) but pre-sent only a selection of these in our main text(see Supplementary Material for additionalresults).In a fully time-varying Pradel seniority

model, survival and sampling in the last timeinterval (given by piwi−1, with i in this casebeing the last time interval) and seniority andsampling in the first time interval are not separ-ately identifiable (Connolly and Miller 2001b).To obtain estimates for survival, seniority,and sampling probabilities for all of the Ordo-vician, we include two Cambrian time binsbefore and two Silurian after the first and lastOrdovician stages, respectively. In that waywe avoid the described boundary effects.Note that for the time-constant model, weonly use occurrence data from the Ordovician,because there are no boundary effects andbecause we are only interested in comparingOrdovician probabilities.

Genus Richness.—We estimated genus rich-ness using the POPAN model (Schwarz andArnason 1996). In contrast to the closed-population approach of the Pradel senioritymodel, the POPAN model is an open-population approach (Schwarz and Arnason1996). This means that individuals (genera inour case) can enter the observed population(global or regional community in our case)from a superpopulation. In our context, thesuperpopulation (N ) is the number of generaavailable to be sampled that may or may notbe sampled throughout the whole study per-iod, where N = ∑i−1

0 Bi (Schwarz and Arnason1996). Here, Bi is the number of new genera ori-ginating between two time intervals (numberof births in the original description ofPOPAN). It is estimated by Bi = penti−1N,where pent is the probability of enteringthe pool of genera. The genus richness ineach time interval is then Ni =Ni−1wi−1 + Bi

(Schwarz and Arnason 1996), where wi−1 isthe survival probability into the time intervalin focus. Similar to the edge effect describedabove, wi−1 cannot be estimated independentlyin a fully time-varying POPAN model. This isalso true for the parameters N1, Nmax, pent1,and pentmax−1. Thus, we include additional

time bins before and after the Ordovician, asdone for the Pradel seniority model.

Laurentia and Baltica.—To assign the obser-vations of genera documented in the PBDB topaleocontinents, we looked up their geoplatecode from Müller et al. (2008), which isprovided in the PBDB, and then assignedthese to either Baltica or Laurentia usingCocks and Torsvik (2004) and Torsvik andCocks (2016a,b) for guidance. Note that insome cases, geoplate codes were not assignedin the PBDB. In those cases, we used country(cc) or state, encoding modern positions, forassignments to paleocontinents in PBDB. Weprovide our assignments in the SupplementaryMaterial. Some genera were observed as“endemic” to Baltica (194 genera) or Laurentia(731 genera), while others were describedfrom both paleocontinents (480 genera). Werestricted our analyses to those genera thatwere observed only on either one of the paleo-continents in question. “Endemic” is in quota-tion marks, because we assume that generaare found only where they are observed, andwe do not explicitly model migration.We note that 33% of the Baltic genera are

arthropods, while 18% are brachiopods and16% are mollusks. The remaining 33% of theBaltic genera are bryozoans, echinoderms, cni-darians, chordates, annelids, hemichordates,and others. Of the Laurentian genera, 25% arearthropods, 21% are mollusks, and 19% areechinoderms. The remaining 35%of Laurentiangenera are bryozoans, brachiopods, poriferans,cnidarians, chordates, and others. Moredetailed information on the representation ofdifferent phyla in the data subsets can befound in Supplementary Tables S6–S8 in theSupplementary Material.

Onshore–Offshore.—For our comparison ofonshore and offshore areas, we assign generausing information on depositional environ-ments given in the PBDB (see SupplementaryMaterial for details). Roughly speaking, weconsider onshore environments as thoseabove fair-weather wave base in high-energyenvironments and offshore environments asthose below stormwave base representing low-energy environments. We only consider generathat have their first occurrence record in eitheronshore (532 genera) or offshore (396 genera)

FRANZISKA FRANECK AND LEE HSIANG LIOW4

areas, regardless of the locations of their subse-quent observations. This means that extinctionrates that are estimated with these data arenot representative for the actual extinctionthat happens in onshore and offshore areas,respectively, because taxa may have migratedand became extinct somewhere else. To esti-mate extinction rates for onshore and offshoreareas, we considered genera that have theirlast occurrence records in either onshore (537genera) or offshore (411 genera) areas, regard-less of the locations of their prior observations.In doing so, we assume that these first and lastpaleoenvironments of observations are thesame as those where they actually originatedor went extinct.The analyses were done with the program

MARK (White 2016) via the RMark interfacefor R (Laake 2013).

Results

Global origination rates are similar to extinc-tion rates between the Tremadocian andDapin-gian (Fig. 1A). At the Dapingian/Darriwilianboundary, the global origination rate is muchhigher than the extinction rate, which alsodropped perceptibly compared with the earlierOrdovician. Extinction and origination ratesbecome similar again before the Hirnantianmass extinction (Fig. 1A).The resulting net diversification is negative

between the Tremadocian and Dapingian, cor-responding to the extinction rates being slightlygreater than origination rates during these timeintervals (Fig. 1B). Between the Dapingian andDarriwilian, net diversification dramaticallyincreases, with the number of genera doubled.Net diversification is lower again thereafter(i.e., close to zero), before it becomes negative,driven by the high extinction rate duringthe Hirnantian mass extinction. Estimates ofgenus richness largely correspond to thechanges in net diversification changes(Fig. 1B), despite different assumptions of“population closure” used to estimate diversifi-cation and richness (see “Methods”). Forexample, net diversification rate between theDapingian and Darriwilian is about 1; henceit follows that the point estimate of the numberof genera about doubled from 900 in the

Dapingian to 1900 in the Darriwilian. Afterthe increase in the Darriwilian, genus richnessstays relatively high until theHirnantian extinc-tion. There is an average increasing trend insampling rates throughout the Ordovician(Fig. 1C).Origination probabilities for Baltica are 0.190

(95% CI 0.155, 0.230) per million years for thewhole Ordovician, while Laurentian origin-ation probabilities are 0.088 (95% CI 0.079,0.097), given a Pradel seniority model thatimposes constant origination, extinction, andsampling probabilities through time. Extinctionprobabilities, estimated with the same time-constant model, are 0.169 (95% CI 0.134,0.211) for Baltica and 0.069 (95% CI 0.061,0.080) for Laurentia. Net diversification prob-abilities are 0.026 (95% CI 0.014, 0.038) forBaltica and 0.020 (95% CI 0.014, 0.025) forLaurentia.Baltica shows greater interval-to-interval ori-

gination rates than Laurentia throughout theOrdovician (Fig. 2A). At the Tremadocian/Floian and Dapingian/Darriwilian boundar-ies, origination rates are at their highest on Bal-tica. On Laurentia, origination rates are at theirhighest at the Cambrian/Tremadocian andDapingian/Darriwilian boundaries. Note thatvariation in estimates and their 95% confidenceintervals is much greater until the Dapingian/Darriwilian boundary (see also SupplementaryFig. S7). However, after the Dapingian/Darri-wilian boundary, Baltic origination rates areconsistently higher than Laurentian ones.From the Tremadocian/Floian boundary

and thereafter, extinction rates are higher onBaltica than on Laurentia (Fig. 2B). On bothpaleocontinents, extinction rates decrease onaverage from the Tremadocian/Floian bound-ary until the Darriwilian/Sandbian boundary.Thereafter they show an increasing trend.Note that the 95% confidence intervals forextinction rates are largely overlapping forthe two paleocontinents until the Dapingian/Darriwilian boundary (cf. SupplementaryFig. S7). Thereafter, Baltic extinction rates areconsistently higher than Laurentian extinctionrates.As a result of the extinction and origination

rates (Fig. 2A,B), net diversification rates aregreater on Baltica than on Laurentia at the

DIVERSIFICATION DYNAMICS OF THE GOBE 5

Tremadocian/Floian boundary (Fig. 2C). Atthe Floian/Dapingian boundary, net diversifi-cation rates are slightly greater on Laurentiathan on Baltica. Thereafter, net diversificationrates are slightly greater on Baltica than onLaurentia, until the Katian/Hirnantian bound-ary, although 95% confidence intervals areoverlapping between the two paleocontinentsthroughout.Sampling rates increase on average from the

Floian to the Hirnantian for Laurentia(Fig. 2D). Sampling rates for Baltica can onlybe estimated from the Darriwilian onward,during which sampling rates are lower onBaltica compared with Laurentia.Baltica had relatively low genus richness in

the Early and early Middle Ordovician (Trema-docian to Dapingian) (Fig. 3). Laurentia hadgreater genus richness than Baltica during thesame time, although the trajectories of both

paleocontinents are very similar. The peak innet diversification (cf. Fig. 2) is expressed as afivefold increase of genus richness on Balticaand an almost threefold increase on Laurentiabetween the Dapingian and Darriwilian. Thisresults in an increase from about 13 to 64 generaon Baltica, and from about 99 to 286 generaon Laurentia for the higher taxa we examined.Although the first substantial increase ingenus richness happened at the Dapingian/Darriwilian boundary, net diversification ratesclose to or slightly above zero until theKatian/Hirnantian boundary (Fig. 2C) led toan Ordovician peak in genus richness duringthe Katian (Fig. 3).Origination and extinction rates in onshore

and offshore areas are barely distinguishablethroughout the Ordovician. Onshore origin-ation probabilities are 0.069 (95% CI 0.060,0.079) per million years for the whole

Fig.

1-B/W

onlin

e,B/W

inprint

FIGURE 1. Global genus diversification and genus diversity dynamics. A, Origination (solid line and solid circles, O) andextinction (dotted line and open circles, E) rates as events per million years (Myr). B, Net diversification rate (solid line andtriangles) and genus richness (dotted line and rectangles). Horizontal gray line represents zero net diversification. C, Sam-pling events per million years (Myr). Vertical lines are 95% confidence intervals. Stage abbreviations: Tr, Tremadocian; Fl,Floian; Dp, Dapingian; Dw, Darriwilian; Sa, Sandbian; Ka, Katian; Hi, Hirnantian.

FRANZISKA FRANECK AND LEE HSIANG LIOW6

Ordovician, while offshore origination prob-abilities are 0.060 (95% CI 0.052, 0.070), givena Pradel seniority model that imposes constantorigination, extinction, and sampling probabil-ities through time. Extinction probabilities forthe whole Ordovician, using the reversed dataset but the same model, are 0.070 (95% CI0.058, 0.085) for onshore areas and 0.085 (95%CI 0.069, 0.104) for offshore areas.Interval-to-interval origination rates in

onshore and offshore areas are very similarthroughout most of the Ordovician, given atime-varying Pradel seniority model with sep-arate estimates for onshore and offshore taxa(Fig. 4). After the Cambrian/Tremadocianboundary, onshore rates, which start higherthan offshore rates, converge. At the

Fig.

2-B/W

onlin

e,B/W

inprint

FIGURE 2. Genus diversification dynamics on Baltica and Laurentia. A, Origination rates as events per million years (Myr).B, Extinction rates as events per million years (Myr). C, Net diversification rates where the horizontal line represents zeronet diversification. D, Sampling rates as events per million years (Myr). Vertical lines represent 95% confidence intervals inA to D. Baltic rates (B) are indicated by solid lines and circles, while Laurentian rates (L) are indicated by dashed lines andtriangles. Stage abbreviations as in Fig. 1. Estimated probabilities or confidence intervals thereof that are one or zero areindications of poorly constrained estimates and are hence removed from the plots. Net diversification rates with confidenceintervals spanning more than 10 are also removed for the same reason.

Fig.

3-B/W

onlin

e,B/W

inprint

FIGURE 3. Genus diversity dynamics on Baltica (B) andLaurentia (L). Estimated genus richness on Laurentia(dashed line, triangles) and Baltica (solid line, circles)based on the POPAN model. Stage abbreviations as inFig. 1. Vertical lines represent 95% confidence intervals.

DIVERSIFICATION DYNAMICS OF THE GOBE 7

Dapingian/Darriwilian boundary, originationrates are high in both paleoenvironments,reflecting the global dynamics at that time.Until the Floian/Dapingian boundary,

extinction rates are higher in onshore areasthan in offshore areas (Fig. 4B). At the Dapin-gian/Darriwilian boundary, extinction ratesfrom onshore and offshore areas are similar,with greatly overlapping confidence intervals.Thereafter, until the Katian/Hirnantian bound-ary, extinction rates are higher in offshore thanin onshore areas.For diversification and sampling rates, based

on first and last observations in either onshoreor offshore areas, which are not central for

our hypothesis, see Supplementary Material(Supplementary Figs. S9 and S10).In this study we are specifically interested in

changes of diversification rates on differentpaleocontinents or onshore/offshore areasthrough time. Therefore, we choose to presentresults from the fully time-varying model forall parameters and covariates. For complete-ness, we tested the fit of different models withdifferent parameter specifications throughtime by comparing their Akaike informationcriterion values. Results of these model com-parisons can be found in the SupplementaryMaterial (Supplementary Tables S1–S4).

Discussion

Global Ordovician Dynamics.—We confirmed,by explicitly modeling incomplete sampling,that the increase of genus richness during theOrdovician was very rapid around the Dapin-gian/Darriwilian boundary, as suggested bymany authors, including Servais et al. (2009),Hints et al. (2010), Harper et al. (2013), Rasmus-sen et al. (2016), and Trubovitz and Stigall(2016). However, this increase could havebeen driven by a lowered extinction rate and/or a higher origination rate. Here, we showfor the first time, that global origination ratesfor the Ordovician peaked at the Dapingian/Darriwilian boundary, right before the spikein genus richness during the Darriwilian(Fig. 1). In addition, the extinction rate at thesame boundary is slightly lower than in theprevious boundary (Floian/Dapingian bound-ary). Net diversification rates were in fact closeto or lower than zero before the Dapingian/Darriwilian boundary, after which theyrocketed up with a doubling of genera (fromc. 800 to c. 1900 genera; Fig. 1) during the Dar-riwilian. This doubling of genera is greater thanwhat was inferred recently by Kröger (2017)using a similar approach. Kröger estimated a1.4 times increase in genus richness over thesame time period (see Kröger 2017), althoughhis genus richness estimate for the Darriwilian(ca. 2000) is similar to ours (ca. 1900). In add-ition, Kröger’s maximum genus richness forOrdovician stages stands at ca. 2200 generaduring the Katian, in contrast to ours, whichoccurs at the Darriwilian. These differences,

Fig.

4-B/W

onlin

e,B/W

inprint

FIGURE 4. Genus origination and extinction rates inonshore and offshore areas. A, Origination rates as eventsper million years (Myr), based on first observation in eitheronshore or offshore areas. B, Extinction rates as events permillion years (Myr) based on last observation in eitheronshore or offshore areas. Vertical lines represent 95% con-fidence intervals in A and B. Onshore rates (on) are indi-cated by solid lines and circles while offshore rates (off)are indicated by dashed lines and triangles. Stage abbrevia-tions as in Fig. 1. Estimated probabilities or confidenceintervals thereof that are one or zero are indications ofpoorly constrained estimates and are hence removed fromthe plots. Net diversification rates with confidence intervalsspanning more than 10 are also removed for the samereason.

FRANZISKA FRANECK AND LEE HSIANG LIOW8

despite our using the same model for genusrichness inference, might be due to differentialtemporal assignments of genus records fromthe PBDB via RNames in the Kröger study.RNames (Kröger and Lintulaakso 2017) is adynamic interface that correlates selected strati-graphic opinions with the purpose of increas-ing stratigraphic resolution. Dividing stagesinto stage slices reduces the number of observa-tions per time bin, possibly depleting somestage slices of data, so confidence intervals ofthe estimates would subsequently increase,especially for our paleocontinental and paleo-environmental analyses. The increases in confi-dence intervals would be even more severe ifobservations are restricted to specific paleocon-tinents or bathymetric groups. In addition, therules by which stages are subdivided intostage slices in RNames are currently not well-documented enough for our use. For thesereasons, we estimated diversification rates ona coarser time resolution, but with betterunderstood data for the benefit of more confi-dent estimates. There is some concern thatbias is introduced by assigning fossil occur-rences to global stages when the occurrenceswere originally associated with regional stages.However, our sensitivity analyses show thatreducing the data set to only fossil occurrencesassigned to global stages does not change ourqualitative inferences (Supplementary Fig. S6in the Supplementary Material).In their pioneering global study, Connolly

and Miller (2001b) simultaneously estimatedorigination, extinction, and sampling probabil-ities for the Ordovician. They found that bothorigination and extinction probabilities havehigher values approximately around the Darri-wilian, although they found no exceptionaldiversification peak (Connolly and Miller2001b), in contrast to what we found. WhileConnolly and Miller (2001b) used the samemodel we did, they estimated origination andextinction probabilities between time intervalsof equal length, because probabilities of eventsover unequal time intervals cannot be directlycompared. Rather than forcing these data toconform to geologically unnatural but equaltime intervals, we used unequal but geologic-ally natural Ordovician stages, but we con-verted probabilities into rates (see “Methods”).

The general diversification trends estimated inConnolly and Miller may also differ from oursdue the broader set of marine invertebratesused in our estimation. For completeness, wedivided our data set into subsets of those taxaConnolly and Miller (2001a) studied (seeSupplementary Figs. S12, S15–S17). We findthat the dynamics of these taxa broadly con-form to the global patterns we have estimated.However, others have shown that graptolites(Cooper et al. 2014) and echinoderms (Sprinkleand Guensburg 1995, 2004), unlike the taxa weinvestigated (arthropods, brachiopods, andmollusks; see Supplementary Material), showan increase in genus richness during the EarlyOrdovician. Given that the model used inConnolly and Miller (2001b) and this studyexplicitly accounts for sampling probabilities,we do not expect the addition of more observa-tions (of correctly identified anddated samples)to change the estimates of mean extinctionand origination considerably, but to increasethe sampling probabilities while tighteningthe confidence intervals for extinction andorigination.As already mentioned, many hypotheses

have been raised for why diversification rateswere so high during the GOBE, some ofwhich likely acted more globally and othersmore regionally. While our global estimatesintegrate over the processes that occur at localto global levels, details of regional dynamicsgive us clues as to what types of processesmight be operating. In other words, if theGOBE in different regions is driven by differentfactors, we would expect diversificationdynamic patterns to be different. For instance,if increased sedimentary input influenceddiversification rates, the rates of taxa closest tovolcanically and tectonically active areas mayexperience more changes than those in theoceans farther away, all other things beingequal. To explore the contrast between globaland regional controls of Ordovician diversifica-tion, we examine the dynamics on Laurentiaand Baltica and in onshore and offshore areasand discuss these in relation to our globalestimates.

Contrasting Laurentia and Baltica.—It is strik-ing that the peaks in origination rates happenedon both Baltica and Laurentia between the

DIVERSIFICATION DYNAMICS OF THE GOBE 9

Dapingian and the Darriwilian (Fig. 2), a pro-cess that led to the largest increase in genusrichness over the Ordovician at the Darriwilianfor both continents. Prior to this peak, origin-ation and extinction rates appear to be uncoor-dinated on the two paleocontinents (see alsoSupplementary Fig. S7). After the Dapingian/Darriwilian boundary, changes in diversifica-tion dynamics appear to be more coordinated.Based on this observation, we suggest that wecan subdivide Ordovician diversification intothree different phases. In the first phase (theEarly Ordovician: Cambrian/Tremadocianand Tremadocian/Floian boundaries), the vari-ation in diversification rates seems relativelyuncoordinated on Baltica and Laurentia. Inthe second phase (the Middle Ordovician:Floian/Dapingian and Dapingian/Darriwilianboundaries), origination rates peak dramatic-ally on both paleocontinents. In the last phase(the Late Ordovician: Darriwilian/Sandbianto Katian/Hirnantian boundaries), diversifica-tion rates seem to change in concert on thetwo paleocontinents. The three phases hint atregional effects on diversification beingstronger in the Early Ordovician, and globaleffects being stronger in the Middle to LateOrdovician. We note in passing that ouronshore and offshore data subsets appear alsoto be more uncoordinated before the Dapin-gian/Darriwilian boundary than after that,just like the dynamics we estimated for thetwo paleocontinents.In the EarlyOrdovician, Laurentiawas stably

situated close to the equator, while Baltica wasrotating from the southernmidlatitudes towardlower latitudes (Torsvik and Cocks 2016a),moving through different climatic zones.Active volcanism occurred during the wholeOrdovician (Barnes 2004), accompanied bygreat siliciclastic input in adjacent areas (Ser-vais et al. 2009), especially on the eastern sideof Laurentia, where the Taconic orogeny hadstarted during theMiddle Ordovician (Hollandand Patzkowsky 1996; Novack-Gottshall andMiller 2003). This greater siliciclastic inputpurportedly led to a greater genus richness onLaurentia (Miller 1997a). The increase ingenus richness from the Dapingian to theDarriwilian common to Laurentia and Balticacorroborates previous observations restricted

to specific organismal groups. For instance,Trubovitz and Stigall (2016) found a peak inbrachiopod species richness on both Balticaand Laurentia in the middle Darriwilian byusing range-through data compiled by Ras-mussen et al. (2007). Similarly, Paris et al.(2004) recorded the onset of the GOBE inchitinozoans at the Dapingian/Darriwilianboundary on both Baltica and Laurentia,based on range-through data. It is noteworthythat their actual peak of Laurentian chitinozo-ans was found in the early Late Ordovician,while the Baltic peak was detected spanningfrom the Darriwilian to the early Sandbian(Paris et al. 2004). These findings are similar toour finding that peak genus richness occurredin the Katian Laurentia and Baltica (Fig. 3).While the diversification dynamics on Laur-

entia and Baltica are broadly similar after theDapingian/Darriwilian boundary, there arealso differences between the two paleoconti-nents. At the Tremadocian/Floian boundary,there appear to be peaks in both originationand extinction rates on Baltica that are notexpressed on Laurentia. Given the size of the95% confidence intervals (see also Supplemen-tary Fig. S7), we refrain from overinterpretingthese observations. However, these peaksmay indicate changes on Baltica before theDapingian/Darriwilian peak that enhancedincreased turnover, although this did not resultin an increase in genus richness.The abovementioned regional effects could

have been dominating factors in the earlyOrdovician, while globally acting changescould have contributed to a coordinatedincrease of origination rates on Baltica andLaurentia during the GOBE (i.e., starting inthe Dapingian and continuing into the Darriwi-lian). One such global change suggested as adriver of the GOBE is the proposed coolingthat began during theMiddle Ordovician (Trot-ter et al. 2008; Rasmussen et al. 2016) and wassustained until the Late Ordovician (e.g., Saltz-man and Young 2005; Trotter et al. 2008). Thesuggested timing of the onset of cooling fitsbroadly with the increase in origination ratesthat we have found in our study. Frequentasteroid impacts during the Early and MiddleOrdovician represent another worldwide con-dition that would have been experienced by

FRANZISKA FRANECK AND LEE HSIANG LIOW10

the Ordovician seas (Schmitz et al. 2001), andthese extraterrestrial inputs have also beenlinked to GOBE (Schmitz et al. 2008). Thisasteroid-driven GOBE hypothesis has recentlybeen refuted on the basis of refined timings ofthese impacts using new isotopic data (Linds-kog et al. 2017), but we argue that we cannotcompletely reject this hypothesis before wehave temporal estimates of diversification thatare also more highly resolved.Ecological theory and contemporary empir-

ical studies have shown that larger terrestrialareas can harbor more species than smallerareas (e.g., MacArthur and Wilson 1967;Rosenzweig 1995). However, this relationshipis less clear for the marine realm (Roy et al.1998; Valentine 2009), in part due to fluidboundaries. Despite uncertainties, we werestill curious as to whether we could detect agreater total genus richness on Laurentia thanBaltica (as found by Miller 1997a), given thatcircumstantial evidence indicates that Lauren-tia was much larger than Baltica (Torsvik andCocks 2016a). Here, we assume, as in manypaleontological studies (e.g., Sepkoski 1991;Finnegan and Droser 2005), that we can usegenus richness as a proxy for species richness.The estimated genus richness for the Ordovi-cian differs quite substantially between thetwo paleocontinents (Laurentia, 646 genera[95% CI 627, 683]; Baltica, 206 genera [95% CI185, 294]), supporting our naive expectation.In addition, there is also temporal variationthat is not coordinated through time (Fig. 3).We restricted our paleocontinental analyses

to genera that were observed on either of thepaleocontinents but not both. In doing so inour analysis framework, we assumed that thegenera in question actually originated on theirassigned paleocontinents and that there areno unobserved occurrences on other paleocon-tinents prior to our first observations. We areaware that this assumption might be violatedfor some genera, but the Pradel senioritymodel does not consider observed or unob-served migration. In addition, we want toemphasize that while the Pradel senioritymodel assumes a closed population, thePOPAN model assumes an open population.This may explain why the POPAN-estimatedgenus richness on Laurentia continuously

increases substantially between Darriwilianand Katian, despite the Pradel-estimated netdiversification rates on Laurentia only beingslightly above zero.

Contrasting Onshore–Offshore Environments.—In addition to examining paleocontinentaldifferences, we also explored originationdynamics in two contrasting environments(onshore and offshore) in order to understandwhat may influence diversification rates. Inaddition to differing energy levels, sea-levelchanges may also more greatly affect onshoreareas than offshore areas (Holland and Christie2013).Jablonski suggested that origination at the

genus level should occur mostly where thehigher-level taxa in question were alreadyestablished (Jablonski et al. 1983; Jablonski2005), while Tomašových et al. (2014) foundevidence, using data from the Eocene and Plio-Pleistocene, that genus origination and extinc-tion rates in onshore areas are greater thanthose in offshore areas. We note that Ordovi-cian origination and extinction rates are onlyminutely different between on- and offshoreenvironments (Fig. 4), results that aremore con-sistent with Jablonski’s hypotheses than withTomašových’s. Analyses based on model selec-tion giving extra support for the similarity inorigination rates between onshore and offshoreareas are presented in the SupplementaryMaterial.In comparing onshore and offshore genus

origination rates, we had to assume that anyunobserved occurrences preceding the firstrecord of the genus in question in a given envir-onment are in the same environment as the firstrecord. Given the incomplete temporal sam-pling of any genus, we realize this may not bea robust assumption, but we lack the tools todeal with this uncertainty at this time. How-ever, given that we discarded genera with mul-tiple paleoenvironmental associations in theirfirst time interval of observation in the PBDB,we believe that “rogue” genera that occur in dif-ferent environments before their first observa-tion are rare. An additional caveat is thatenvironmental classifications in the PBDB arenot clearly defined, such that anyone enteringdata into the PBDBmay have tomake a subject-ive decision as to which environmental

DIVERSIFICATION DYNAMICS OF THE GOBE 11

classification to assign to the fossil in question.As a result of uncertainty, many environmentalassignments end up in the “indet.” (indeter-minate) category. The onshore and offshoredata set we used is quite a lot smaller thanwhat was potentially available (see Supple-mentary Material). However, we have no rea-son to suspect that data points for whichenvironment is marked “indet.” in the PBDBare biased toward any of the two environmentsin which we are interested. We are also awarethat our division of onshore and offshore envir-onments is more conservative than otherspublished (e.g., Bottjer and Jablonski 1988)and that a different subset of data mightsuggest different results.

Conclusions

The global increase in genus richness at theDapingian/Darriwilian boundarywas the resultof a dramatic increase in origination rates, whileextinction rates stayed at relatively low levels.This global increase in origination rates ismirrored on Laurentia and Baltica, as well as inonshore and offshore areas, pointing toward aglobal mechanism behind the peak in origin-ation rates at theDapingian/Darriwilian bound-ary, which is likely the greatest contributor to theGOBE. Based on the patterns of paleocontinentaland paleoenvironmental diversification dynam-ics, it appears that regionally varying factorswere prominent during the Early Ordovician,while globally acting controlling factors appearto have been dominant during the MiddleOrdovician and onward. All else being equal,our results suggest that origination probabilitiesare slightly greater in areas exposed to greaterenvironmental change (i.e., greater disturbancethrough sea-level changes or continentalmovement).

Acknowledgments

This work was funded by the NFR project235073/F20 (principal investigator: L.H.L.).We thank A. Tomašových for helpful com-ments on the division of onshore and offshoreclasses and J. J. Czaplewski, T. Torsvik, andG. Shephard for help with GPlates. F.F. isgrateful to C. Syrowatka, J. Starrfelt,

K. L. Voje, T. Reitan, P. Smits, J. P. Nystuen, S.Finnegan, and B.Kröger for discussions. Wethank J. Crampton, A.Miller, and two anonym-ous reviewers for their constructive feedbackand comments that helped improve this article.We also want to thank all those who contribu-ted primary literature and data to the PBDBand the members of the PBDB for providingdata for our analysis. This article is a contribu-tion to IGCP Project 653: “The Onset of theGreat Ordovician Biodiversification Event.”This is PBDB publication number 331.

Literature CitedAlroy, J., M. Aberhan, D. J. Bottjer, M. Foote, F. T. Fürsich, P.J. Harries, A. J. W. Hendy, S. M. Holland, L. C. Ivany,W. Kiessling, M. A. Kosnik, C. R. Marshall, A. J. McGowan, A.I. Miller, T. D. Olszewski, M. E. Patzkowsky, S. E. Peters,L. Villier, P. J. Wagner, N. Bonuso, P. S. Borkow, B. Brenneis, M.E. Clapham, L. M. Fall, C. A. Ferguson, V. L. Hanson, A.Z. Krug, K. M. Layou, E. H. Leckey, S. Nurnberg, C. M. Powers,J. A. Sessa, C. Simpson, A. Tomašových, and C. C. Visaggi.2008. Phanerozoic trends in the global diversity of marine inver-tebrates. Science 321:97–100.

Barnes, C. R. 2004. Was there an Ordovician superplume event?Pp. 77–80 in Webby et al. 2004.

Bassett, D., K. G. MacLeod, J. F. Miller, and R. L. Ethington. 2007.Oxygen isotopic composition of biogenic phosphate and thetemperature of Early Ordovician seawater. Palaios 22:98–103.

Bergström, S. M., X. Chen, J. C. Gutiérrez-Marco, and A. Dronov.2009. The new chronostratigraphic classification of the Ordovi-cian System and its relations to major regional series and stagesand to δ13C chemostratigraphy. Lethaia 42:97–107.

Botting, J. P. 2002. The role of pyroclastic volcanism in Ordoviciandiversification. In J. A. Crame and A. W. Owen, eds. Palaeobio-geography and biodiversity change: the Ordovician and Meso-zoic–Cenozoic radiations. Geological Society of London SpecialPublication 194:99–113.

Bottjer, D. J., and D. Jablonski. 1988. Paleoenvironmental patternsin the evolution of post-Paleozoic benthic marine invertebrates.Palaios 3:540–560.

Cocks, L. R. M., and T. H. Torsvik. 2004. Major terranes in theOrdovician. Pp. 61–67 in Webby et al. 2004.

——. 2006: European geography in a global context from theVendian to the end of the Palaeozoic. In D. G. Gee andR. A. Stephenson, eds. European lithosphere dynamics.Geological Society of London Memoir 32:83–95.

Connolly, S. R., and A. I. Miller. 2001a. Global Ordovician faunaltransitions in themarine benthos: proximate causes. Paleobiology27:779–795.

——. 2001b. Joint estimation of sampling and turnover rates fromfossil databases: capture-mark-recapture methods revisited.Paleobiology 27:751–767.

——. 2002. Global Ordovician faunal transitions in the marinebenthos: ultimate causes. Paleobiology 28:26–40.

Cooper, R. A., P. M. Sadler, A. Munnecke, and J. S. Crampton.2014. Graptoloid evolutionary rates track Ordovician–Silurianglobal climate change. Geological Magazine 151:349–364.

Finnegan, S., and M. L. Droser. 2005. Relative and absolute abun-dance of trilobites and rhynchonelliform brachiopods across theLower/Middle Ordovician boundary, eastern Basin and Range.Paleobiology 31:480–502.

FRANZISKA FRANECK AND LEE HSIANG LIOW12

Harper, D. A. T. 2006. The Ordovician biodiversification: setting anagenda for marine life. Palaeogeography, Palaeoclimatology,Palaeoecology 232:148–166.

Harper, D. A. T., C. M. Ø. Rasmussen, M. Liljeroth, R. B. Blodgett,Y. Candela, J. Jin, I. G. Percival, J. Rong, E. Villas, and R. Zhan.2013. Biodiversity, biogeography and phylogeography of Ordo-vician rhynchonelliform brachiopods. 1. In D. A. T. Harper andT. Servais, eds. Early Palaeozoic biogeography and palaeogeog-raphy. Geological Society of London Memoir 38:127–144.

Harper, D. A. T., and T. Servais, eds. 2013. Early Palaeozoic bio-geography and palaeogeography: towards a modern synthesis.Geological Society of London Memoir 38:1–4.

Hints, O., A. Delabroye, J. Nõlvak, T. Servais, A. Uutela, andÅ. Wallin. 2010. Biodiversity patterns of Ordovician marinemicrophytoplankton from Baltica: comparison with other fossilgroups and sea-level changes. Palaeogeography, Palaeoclimat-ology, Palaeoecology 294:161–173.

Holland, S. M., and M. Christie. 2013. Changes in area of shallowsiliciclastic marine habitat in response to sediment deposition:implications for onshore–offshore paleobiologic patterns. Paleo-biology 39:511–524.

Holland, S. M., andM. E. Patzkowsky. 1996. Sequence stratigraphyand long-term paleoceanographic change in the Middle andUpper Ordovician of the eastern United States. In B. J. Witzke,G. A. Ludvigson, and J. Day, eds. Paleozoic sequence stratig-raphy: views from the North American craton. Geological Societyof America Special Paper 306:117–129. Geological Society ofAmerica, Boulder, Colo.

Jablonski, D. 2005. Evolutionary innovations in the fossil record:the intersection of ecology, development, and macroevolution.Journal of Experimental Zoology 304B:504–517.

Jablonski, D., J. J. Sepkoski, D. J. Bottjer, and P. M. Sheehan. 1983.Onshore–offshore patterns in the evolution of Phanerozoic shelfcommunities. Science 222:1123–1125.

Kröger, B. 2017. Changes in the latitudinal diversity gradient duringthe great Ordovician biodiversification event. Geology 46:44–47.

Kröger, B., and K. Lintulaakso. 2017. RNames, a stratigraphicaldatabase designed for the statistical analysis of fossil occur-rences—the Ordovician diversification as a case study. Palaeonto-logia Electronica 20.1.1T:1–12.

Laake, J. L. 2013. RMark: An R Interface for Analysis of Capture-Recapture Data with MARK. AFSC Processed Report 2013-01.Alaska Fisheries Science Center, NOAA, National Marine Fisher-ies Service, Seattle, Wash.

Lindskog, A., M.M. Costa, C. M. Ø. Rasmussen, J. N. Connelly, andM. E. Eriksson. 2017. Refined Ordovician timescale reveals nolink between asteroid breakup and biodiversification. NatureCommunications 8:14066.

Liow, L. H., and J. D. Nichols. 2010. Estimating rates and probabil-ities of origination and extinction using taxonomic occurrencedata: capture-mark-recapture (CMR) approaches. In J. Alroyand G. Hunt, eds. Quantitative methods in paleobiology.Paleontological Society Papers 16:81–94.

Liow, L. H., T. Reitan, and P. G. Harnik. 2015. Ecological interac-tions on macroevolutionary time scales: clams and brachiopodsare more than ships that pass in the night. Ecology Letters18:1030–1039.

MacArthur, R. H., and E. O. Wilson. 1967. The theory of islandbiogeography. Princeton University Press, Princeton, N.J.

Miller, A. I. 1997a. Comparative diversification dynamics amongpalaeocontinents during the Ordovician radiation. Geobios20:397–406.

——. 1997b. Dissecting global diversity patterns: examples fromthe Ordovician radiation. Annual Review of Ecology andSystematics, 28:85–104.

——. 2004. The Ordovician radiation: toward a new global synthe-sis. Pp. 380–388 in Webby et al. 2004.

——. 2012. The Ordovician radiation: macroevolutionary cross-roads of the Phanerozoic. Pp. 381–394 in Earth and Life. SpringerNetherlands, Dordrecht.

Miller, A. I., and S. R. Connolly. 2001. Substrate affinities of highertaxa and the Ordovician radiation. Paleobiology 27:768–778.

Miller, A. I., and S. Mao. 1995. Association of orogenic activity withthe Ordovician radiation of marine life. Geology 23:305–308.

——. 1998. Scales of diversification and the Ordovician radiation.Pp. 288–310 inM. L. McKinney and J. A. Drake, eds. Biodiversitydynamics: turnover of populations, taxa, and communities. Col-umbia University Press, New York.

Müller, R. D., M. Sdrolias, C. Gaina, and W. R. Roest. 2008. Age,spreading rates, and spreading asymmetry of the world’s oceancrust. Geochemistry, Geophysics, Geosystems 9:Q04006.

Nichols, J. D., and K. H. Pollock. 1983. Estimating taxonomic diver-sity, extinction rates, and speciation rates from fossil data usingcapture–recapture models. Paleobiology 9:150–163.

Novack-Gottshall, P. M., and A. I. Miller. 2003. Comparative geo-graphic and environmental diversity dynamics of gastropods andbivalves during the Ordovician radiation. Paleobiology 29:576–604.

Paris, F., A. Achab, E. Asselin, C. Xiao-Hong, Y. Grahn, J. Nõlvak,O. Obut, J. Samuelsson, N. Sennikov, M. Vecoli, J. Verniers,W. Xiao-feng, and T. Winchester-Seeto. 2004. Chitinozoans.Pp. 294–311 in Webby et al. 2004.

Pope, M. C., and J. B. Steffen. 2003. Widespread, prolonged lateMiddle to Late Ordovician upwelling in North America: aproxy record of glaciation? Geology 31:63–66.

Pradel, R. 1996. Utilization of capture–mark–recapture for the studyof recruitment and population growth rate. Biometrics 52:703–709.

Rasmussen, C.M. Ø., J. Hansen, and D. A. T. Harper. 2007. Baltica: amid Ordovician diversity hotspot. Historical Biology 19:255–261.

Rasmussen, C. M. Ø., C. V. Ullmann, K. G. Jakobsen, A. Lindskog,J. Hansen, T. Hansen, M. E. Eriksson, A. Dronov, R. Frei, C. Korte,A. T. Nielsen, and D. A. T. Harper. 2016. Onset of main Phanero-zoic marine radiation sparked by emerging Mid Ordovicianicehouse. Scientific Reports 6:18884.

Rosenzweig, M. L. 1995. Species diversity in space and time. Cam-bridge University Press, Cambridge.

Roy, K., D. Jablonski, J. W. Valentine, and G. Rosenberg. 1998. Mar-ine latitudinal diversity gradients: tests of causal hypotheses.Proceedings of the National Academy of Sciences USA95:3699–3702.

Saltzman,M. R., and S. A. Young. 2005. Long-lived glaciation in theLate Ordovician? Isotopic and sequence-stratigraphic evidencefrom western Laurentia. Geology 33:109–112.

Schmitz, B., M. Tassinari, and B. Peucker-Ehrenbrink. 2001. A rainof ordinary chondritic meteorites in the early Ordovician. Earthand Planetary Science Letters 194:1–15.

Schmitz, B., D. A. T. Harper, B. Peucker-Ehrenbrink, S. Stouge,C. Alwmark, A. Cronholm, S. M. Bergström, M. Tassinari, andW. Xiaofeng. 2008. Asteroid breakup linked to the great Ordovi-cian biodiversification event. Nature Geoscience 1:49–53.

Schwarz, C. J., and A. N. Arnason. 1996. A general methodologyfor the analysis of capture–recapture experiments in open popu-lations. Biometrics 52:860–873.

Sepkoski, J. J. 1991. A model of onshore–offshore change in faunaldiversity. Paleobiology 17:58–77.

——. 1997. Biodiversity: past, present, and future. Journal ofPaleontology 71:533–539.

Sepkoski, J. J., R. K. Bambach, D. M. Raup, and J. W. Valentine.1981. Phanerozoic marine diversity and the fossil record. Nature293:435–437.

Servais, T., and D. A. T. Harper. 2018. The great Ordovician biodi-versification event (GOBE): definition, concept and duration.Lethaia:1–14.

Servais, T., D. A. T. Harper, J. Li, A. Munnecke, A. W. Owen, and P.M. Sheehan. 2009. Understanding the great Ordovician

DIVERSIFICATION DYNAMICS OF THE GOBE 13

biodiversification event (GOBE): influences of paleogeography,paleoclimate, or paleoecology? GSA Today 19:4–10.

Sprinkle, J., and T. E. Guensburg. 1995. Origin of echinoderms inthe Paleozoic evolutionary fauna: the role of substrates. Palaios10:437–453.

——. 2004. Crinozoan, blastozoan, echinozoan, asterozoan andhomalozoan echinoderms. Pp. 266–280 in Webby et al. 2004.

Tomašových, A., S. Dominici, M. Zuschin, and D. Merle. 2014.Onshore–offshore gradient in metacommunity turnover emergesonly over macroevolutionary time-scales. Proceedings of theRoyal Society of London B 281:20141533.

Torsvik, T. H., and L. R. M. Cocks. 2016a. Ordovician. Pp. 101–123in Earth history and palaeogeography. Cambridge UniversityPress, Cambridge.

——. 2016b. Tectonic units of the Earth. Pp. 38–76 in Earth historyand palaeogeography. Cambridge University Press.

Trotter, J. A., I. S. Williams, C. R. Barnes, C. Lécuyer, and R.S. Nicoll. 2008. Did cooling oceans trigger Ordovician

biodiversification? Evidence from conodont thermometry.Science 321:550–554.

Trubovitz, S., and A. L. Stigall. 2016. Synchronousdiversification of Laurentian and Baltic rhynchonelliformbrachiopods: implications for regional versus global triggersof the great Ordovician biodiversification event. Geology44:743–746.

Valentine, J. W. 2009. Overview of marine biodiversity. Pp. 3–28 inJ. D. Witman and K. Roy, eds. Marine macroecology. Universityof Chicago Press, Chicago.

Webby, B. D., F. Paris, M. L. Droser, and I. G. Percival, eds. 2004.The great Ordovician biodiversification event. Columbia Univer-sity Press, New York.

White, G. C. 2016. MARK: mark and recapture parameter estima-tion. http://www.phidot.org/software/mark.

Zhan, R., and D. A. T. Harper. 2006. Biotic diachroneity during theOrdovician radiation: evidence from South China. Lethaia39:211–226.

FRANZISKA FRANECK AND LEE HSIANG LIOW14