Brown, J.H. (1995) Macroecology. University of Chicago Press,Chicago.

Erwin, D.H. (1993) The Great Paleozoic Crisis. Columbia Univer-sity Press, New York.

Erwin, D.H. (1998) The end and the beginning: recoveries frommass extinctions. Trends in Ecology and Evolution 13, 344–349.

Flessa, K.W. and Jablonski, D. (1996) The geography of evolu-tionary turnover: global analysis of extant bivalves. In: D.Jablonski, D.H. Erwin and J.H. Lipps, eds. Evolutionary paleo-biology, pp. 376–397. University of Chicago Press, Chicago.

Gaston, K.J. and Blackburn, T.M. (1997) Evolutionary age andrisk of extinction in the global avifauna. Evolutionary Ecology11, 557–565.

Jablonski, D. (1995) Extinctions in the fossil record. In: J.H.Lawton and R.M. May, eds. Extinction rates, pp. 25–44.Oxford University Press, Oxford.

Jablonski, D. (1996) Mass extinctions: persistent problems andnew directions. Geological Society of America Special Paper 307,1–9.

McGhee, G.R. (1996) The Late Devonian mass extinction. Colum-bia University Press, New York.

McKinney, M.L. (1997) Extinction vulnerability and selectivity:combining ecological and paleontological views. AnnualReview of Ecology and Systematics 28, 495–516.

Raup, D.M. (1991) Extinction: bad genes or bad luck? Norton, NewYork.

Smith, A.B. and Jeffery, C.H. (1998) Selectivity of extinctionamong sea urchins at the end of the Cretaceous period.Nature 392, 69–71.

2.3.10 Biotic Recovery from Mass Extinctions

D.J. BOTTJER

Introduction

Much work has been directed towards understandingthe causes of mass extinctions, but comparatively littlehas addressed the patterns and processes of recoveryfrom these biotic crises. The work that has been done onrecoveries typically has been constrained by the time resolution available and the taxonomic expertise of thepalaeontologist. Yet the subject of recovery from massextinctions is widely recognized as one that should behigh on the agenda of palaeobiological research. Under-standing how the Earth’s biota has recovered from massextinctions is significant because not only is it necessaryto understand these processes to appreciate life’s bumpyprogression through the Phanerozoic, but it also helps usto appreciate the fragility of the Earth’s ecosystems,which are under constant assault in the modern world.

Perhaps the best illustration of the importance of

recovery intervals in the history of life is providedthrough work done to define and analyse ‘EcologicalEvolutionary Units’. These ‘EEUs’ are distinctive longintervals of geological time in the Phanerozoic history oflife during which benthic palaeocommunities are com-posed of a static array of genera (Boucot 1983; Sheehan1996) (see Section 4.2.1). Originally the marine Phanero-zoic fossil record was subdivided into 12 EEUs (Boucot1983). However, later work has determined that theshort intervals following several of the mass extinctionsare not EEUs, but represent recovery intervals ‘charac-terized by instability, recurrent replacements and reor-ganizations of communities’ (Sheehan 1996, p. 23). These‘intervals of reorganization’ (Sheehan 1996), observableon a Phanerozoic time scale, range from 3 to 8myr long,while EEUs represent intervals of ecological stabilityranging from 30 to 140myr long.

Nine EEUs and five recovery intervals are recognizedin the Phanerozoic, with each of the latter occurring afterone of the ‘Big Five’ mass extinctions (end-Ordovician, end-Devonian, end-Permian, end-Triassic, and end-Cretaceous). Observable recoveries also occurred aftermass extinctions other than the ‘Big Five’ (e.g. Kauffmanand Harries in Hart 1996), but their ecological structureis not sufficiently different to separate them from theEEU in which they occur. Nevertheless, much has beenlearned about recovery processes from these smallermass extinctions, particularly in the Cretaceous at theCenomanian–Turonian boundary (e.g. Kauffman andHarries in Hart 1996; see also other chapters in Hart1996).

In reconstructing recovery processes for EEU recoveryintervals, as well as after other smaller mass extinctions,analysis of palaeoenvironments and palaeoecology canpose difficulties because these times of changing eco-space utilization may not show similar ecological struc-tures to those found in modern environments. Thuswhen studying biotic recovery from mass extinctions, a non-actualistic analytical approach is commonly warranted (Bottjer 1998).

Each recovery from a mass extinction appears to havea unique signature, depending upon the influence ofseveral factors that determine the nature of biotic recovery: (1) the taxonomic effect of the mass extinction,as measured by taxonomic loss (e.g. Hallam and Wignall 1997), as well as the types of organisms thatremain (and their diversity); (2) the effect of the massextinction upon ecological structure, best measured in an overall sense by using the approach of ‘compara-tive evolutionary palaeoecology’ (Bottjer et al. inHart 1996), and exemplified by the system of palaeoeco-logical levels (see Section 4.2.1) (a finer scale of analysisis, however, also possible); (3) whether the environ-mental stress(es) that caused the mass extinction wasconfined to the mass extinction interval, or continued

202 2 The Evolutionary Process

Palaeobiology IIEdited by Derek E.G. Briggs, Peter R. Crowther

Copyright © 2001, 2003 by Blackwell Publishing Ltd

at some reduced level, thus inhibiting the recovery; and(4) the location and size of geographical and environ-mental refugia.

Studies of recovery intervals have shown that a tem-poral structure can be discerned within them, character-ized by differing biotic features. This temporal structurehas been resolved to different degrees, depending upon whether a theoretical approach was taken (e.g.Harries et al. in Hart 1996), or whether a particular mass extinction (e.g. end-Permian, end-Cretaceous) was being studied. In defining the internal structure of a recovery interval, the usual approach (followedherein) has involved the analysis of taxonomic diversitydata. As more is learned, a variety of palaeoecologicaldata will also be incorporated into definitions of recov-ery interval temporal structure. The following temporalstructure combines features from several studies (e.g.Hallam and Wignall 1997): (1) mass extinction — taxo-nomic diversity drops relatively rapidly, as extinctionrate is greater than origination rate; (2) survival or lag —taxonomic diversity ‘levels out’, as extinction rateapproximately equals origination rate; (3) rebound — tax-onomic diversity begins to increase again, with the reappearance of Lazarus taxa, and as origination rate becomes greater than extinction rate; and (4) expan-sion — taxonomic diversity increases at an even greaterrate due to a further increase in origination rate relativeto extinction rate.

The recovery interval is defined as lasting from theend of the mass extinction until after the expansion has commenced. Not all recoveries after mass extinc-tions show this temporal structure, and segments may be absent. Different temporal structures can be found in recoveries depending upon temporal differences (e.g.the rate at which a recovery proceeded, or the time resolution at which the study was done). Different temporal structures may also be documented in differentecosystems after the same mass extinction (e.g. plankticvs. benthic; marine vs. terrestrial). Variations in temporalstructure of a recovery interval may also have a geo-graphical component. Thus, depending upon the focus of a study, different temporal structures for therecovery interval could be defined for the same massextinction.

Two major data collection and analysis methodologieshave been applied to the study of recoveries, termedhere the ‘taxonomic’ and ‘palaeoecological’ approaches.As modern mass extinction studies were pioneered by ataxonomic approach, taxonomic analyses of recoverieshave been the most prevalent (e.g. Hart 1996; Hallamand Wignall 1997).

Taxonomic approaches

Taxonomic data used in the reconstruction of biotic

recoveries from mass extinctions rely on the presence orabsence of taxa with particular phylogenetic/evolution-ary features within a temporal or geographical frame-work. These data are typically retrieved from literatureor museum collections. Much data originally collectedfor biostratigraphic purposes are particularly suitablefor these types of analysis. In developing a vocabu-lary for more precise communication on biotic recover-ies, several different types of taxa have been defined,sometimes with novel yet informative names.1 Lazarus taxa vanish from the stratigraphic recordduring a mass extinction, are not present during part ormost of the recovery, and then reappear in the record(Fig. 2.3.10.1) (Jablonski 1986). The number of Lazarustaxa has been interpreted to indicate the importance ofrefugia during a mass extinction (e.g. Hallam andWignall 1997), or possibly the number of species that didnot go extinct but whose populations reached such lowlevels during the recovery that they produced only rarefossils that are unlikely to be collected (Hallam andWignall 1997).2 Elvis taxa show the same temporal pattern as Lazarustaxa, but are only convergent with, rather than taxo-nomically the same as, morphologically similar pre-extinction taxa (e.g. Hallam and Wignall 1997).

2.3 Macroevolution 203

LIngula (1)

Claraia (2)

Microgastropods (3)

Dinwoody

Griesbachian

Sinbad

Nammalian

Virgin/Thaynes

Spathian

Crinoids (4)

Stromatolites (5)

Fig. 2.3.10.1 Stratigraphic distribution of selected EarlyTriassic biotic recovery taxa, as well as stromatolites (rangelines shown below each label) in strata deposited in neriticenvironments in the western USA, including: (1) a disaster taxon; (2) a progenitor taxon; (3) opportunists; (4) a Lazarus taxon; and (5) a disaster form. Data from theGriesbachian age Dinwoody Formation, the Nammalian ageSinbad Limestone Member of the Moenkopi Formation, theSpathian age Virgin Limestone Member of the MoenkopiFormation, and the Spathian age Thaynes Formation(primarily from Schubert and Bottjer 1992, 1995).

3 Holdover taxa belong to a higher taxon that experi-enced a significant level of loss in the mass extinction.Such taxa survive into the recovery interval, only tobecome extinct in the survival or lag phase (e.g. Hallamand Wignall 1997).4 Bloom taxa experience an evolutionary burst duringthe recovery interval, and then subsequently decline(Hansen 1988).5 Progenitor taxa first evolve during the mass extinctioninterval and survive to ‘seed’ the evolution of dominantgroups during the recovery interval (Fig. 2.3.10.1)(Kauffman and Harries in Hart 1996).

Palaeoecological approaches

Palaeoecological data that are used for the reconstruc-tion of biotic recoveries after mass extinctions includepalaeocommunity and biofabric information as well astaxonomic data with an ecological component. Such dataare not easily extracted from literature or museum col-lections and generally require new field studies. Impor-tant concepts include the following:1 Opportunists (Fig. 2.3.10.1) are taxa that undergo a dramatic increase in abundance during the recoveryinterval (Hallam and Wignall 1997), typically due torelaxation of competition. Opportunists include disastertaxa, which are long-ranging taxa that become unusuallyabundant during the recovery interval (e.g. Hallam andWignall 1997). This definition has been extended toinclude some microbial structures, and stromatolitesfound in Lower Triassic strata have been termed ‘disas-ter forms’ (Schubert and Bottjer 1992).2 Palaeocommunity structure comprises data on commu-nity properties such as diversity, biogeographical distri-bution, species richness, number of ‘Bambachianmegaguilds’ (adaptive strategies defined by life positionand general feeding type; see also Section 4.2.1), andtiering (see also Section 4.1.4) (e.g. Bottjer et al. in Hart1996).3 Biofabrics are those sedimentary structures that arebiologically mediated, and hence contain distinct biolo-gical information. Biofabrics include microbial struc-tures as well as shell beds, trace fossils, and ichnofabric(e.g. Bottjer et al. in Hart 1996).4 Comparative evolutionary palaeoecology provides aframework that allows palaeoecological data frombefore and after the mass extinction to be compared tothat of the recovery interval (Bottjer et al. in Hart 1996).Palaeoecological levels (see Section 4.2.1) is a methodologyof comparative evolutionary palaeoecology that pro-vides a means to scale or rank palaeoecological changeduring major events in life’s history, such as the ecolo-gical changes due to mass extinctions that occur in re-covery intervals. The system of palaeoecological levelsincorporates data from several of the other palaeoeco-

logical approaches listed above to allow evaluation ofecological change at four levels (first-level changes are ofthe greatest magnitude and represent the advent or lossof an ecosystem; second-level changes occur within an established ecosystem and represent major structuralchanges at the largest ecological scale; third-levelchanges include community-scale shifts within an estab-lished ecological structure; fourth-level changes aresimilar in magnitude to most minor ecological changes;see also Section 4.2.1).

Recovery from the end-Permian mass extinction

The end-Permian mass extinction was the largest bioticcrisis of the Phanerozoic, when possibly as many as 90%of species became extinct (see Section 2.4.4) (Hallam andWignall 1997). The magnitude of the mass extinction,and the resulting long recovery interval (7–10myr),makes the recovery of benthic macroinvertebrates fromthis particular crisis more amenable to analysis thanmost. The large biotic effects and long time intervals helpto counter some of the distortions of the fossil and strati-graphic record that are normally present. A variety ofmechanisms have been implicated in the end-Permianmass extinction, including marine anoxia, eruption ofthe Siberian traps, and hypercapnia (CO2 poisoning),and debate continues on whether the crisis representsone event or two in close succession (see Section 2.4.4)(Hallam and Wignall 1997). Whatever the cause, end-Permian environmental conditions wreaked such havocon the Earth’s biota that the Early Triassic has beenviewed as the most profound ‘dead zone’ in thePhanerozoic fossil record, representing an unusuallylong recovery interval (e.g. Hallam and Wignall 1997).Debate on why recovery took so long has centred onthree possibilities: (1) the mass extinction was so exten-sive that an unusually long period of time was involvedin the recovery; (2) environmental stress related to thecauses of the mass extinction continued to occur throughmost of the Early Triassic; and (3) preservation and sam-pling bias has skewed our perception of the fossil record(e.g. Schubert and Bottjer 1995; Erwin and Pan in Hart1996). Although several biostratigraphic schemes havebeen utilized for the Early Triassic (e.g. Hallam andWignall 1997), this interval is commonly divided into the Griesbachian (oldest), Nammalian, and Spathianstages (Fig. 2.3.10.1), which span a total of approximately7–10myr.

The pattern of gastropod occurrence from the Permianinto the Triassic shows a variety of taxa that are absentfrom all or part of the Early Triassic fossil record; this wasthe first example to be recognized of what was laterdefined as the Lazarus effect (e.g. Jablonski 1986; Erwinand Pan in Hart 1996; Hallam and Wignall 1997). Crinoid

204 2 The Evolutionary Process

echinoderms are also absent from the early part of theEarly Triassic fossil record (Fig. 2.3.10.1). If the Lazaruseffect can be extended to the class level, then theCrinoidea is also a Lazarus taxon, with the youngestPermian crinoid in this sequence an inadunate, and theoldest Triassic crinoid an articulate. The Permian/Trias-sic mass extinction is thought to have caused the extinc-tion of all but one genus of crinoids (e.g. Schubert andBottjer 1995).

The Griesbachian commonly contains abundant speci-mens of the bivalve Claraia (Fig. 2.3.10.1), which firstevolved in the latest Permian and then underwent anexplosive evolutionary radiation from the Griesbachianinto the Nammalian, thus giving it the characteristics ofa progenitor taxon (Hallam and Wignall 1997). ManyLower Triassic intervals also contain beds composedalmost entirely of tiny adult gastropods (Fig. 2.3.10.1);these microgastropods acted as opportunists in EarlyTriassic seas (see Section 2.4.4) (Schubert and Bottjer1995; Hallam and Wignall 1997). Subtidal marine stro-matolites are found in Lower Triassic carbonate facies ata variety of localities (e.g. Fig. 2.3.10.1), representingdeposition marginal to the global Panthalassic Oceanand the Palaeo-Tethys (e.g. Schubert and Bottjer 1992;Bottjer et al. in Hart 1996), and these have been termed‘disaster forms’. In the Griesbachian the inarticulate bra-chiopod Lingula is perhaps as abundant worldwide as itis in any Phanerozoic strata (e.g. Fig. 2.3.10.1) (Schubertand Bottjer 1995; Hallam and Wignall 1997), and thislong-ranging genus similarly has all the classic featuresof a disaster taxon.

Other palaeoecological effects of this mass extinctionhave long been known, including the presence of wide-spread cosmopolitanism among Early Triassic taxa (e.g.Hallam and Wignall 1997). Early Triassic palaeocommu-nities are dominated overwhelmingly by bivalves (e.g.Schubert and Bottjer 1995; Hallam and Wignall 1997;Wignall et al. 1998). Only one study of Early Triassic,level-bottom benthic palaeocommunity structure hasbeen carried out, involving Lower Triassic (Nammalian,Spathian) carbonate strata in western North America.The average number of species in collections definingpalaeocommunities in these shelfal settings is 13 (Schubert and Bottjer 1995; Bottjer et al. in Hart 1996).Comparison with data from Permian and later Triassicpalaeocommunities indicates that species richness ofthese Early Triassic palaeocommunities is lower thantypical later Palaeozoic or other Mesozoic palaeocom-munities from equivalent environments (Schubert andBottjer 1995; Bottjer et al. in Hart 1996).

Similarly, of the possible Bambachian megaguilds,only five are occupied in these Early Triassic palaeo-communities from western North America (Schubertand Bottjer 1995; Bottjer et al. in Hart 1996). This is asignificant reduction from the 14 megaguilds typically

found in Palaeozoic faunas, and also contrasts stronglywith the 20 megaguilds commonly found in later Meso-zoic–Cenozoic faunas (see Section 4.2.1) (Bottjer et al.in Hart 1996). Along with reductions in palaeocom-munity species richness and occupation of Bambachianmegaguilds, the end-Permian mass extinction also had adramatic effect upon patterns of tiering (see Section4.1.4). Studied Early Triassic palaeocommunities haveonly the 0 to +5cm epifaunal tier present until theSpathian, when, with the reappearance of crinoids, the+5 to +20cm tier again developed (e.g. Schubert andBottjer 1995; Bottjer et al. in Hart 1996). Infaunal tiering,as indicated by trace fossils, was also strongly affected,with only the 0 to -6cm and -6 to -12cm tiers present instudied Lower Triassic stratigraphic sections (e.g. Schu-bert and Bottjer 1995; Bottjer et al. in Hart 1996; Twitchett 1999). By the Middle Triassic tiering appears tohave recovered to levels found in the late Palaeozoic (seeSection 4.1.4). General studies of trace fossils in theDolomites, Spitsbergen, and western North America(Schubert and Bottjer 1995; Wignall et al. 1998; Twitchett1999) typically show an increase in ichnogeneric diver-sity and the amount of bioturbation as recorded by ichnofabric indices through the Early Triassic, and thisevidence has commonly been taken to indicate the pres-ence of deleterious oxygen-deficient conditions duringthe recovery interval (e.g. Hallam and Wignall 1997;Wignall et al. 1998; Twitchett 1999). If sections in Spits-bergen show the oldest evidence for deeper infaunaltiering in the Early Triassic, as well as earlier Early Trias-sic faunas with appreciable diversity, then recovery fromthis mass extinction may have first begun in higherpalaeolatitudes (Wignall et al. 1998).

The analysis of much of this palaeoecological data in acomparative fashion has shown that ecological condi-tions for this recovery interval (particularly the earlierpart of the Early Triassic) were most like those of the LateCambrian/Early Ordovician (Bottjer et al. in Hart 1996).Further analysis using palaeoecological levels showsthat the Early Triassic recovery represents a major inter-val of ecological change, as great as any other in the Phanerozoic (see also Section 4.2.1). The effects of theend-Permian mass extinction include changes at thesecond, third, and fourth levels. The biggest changes areat the second level, including the loss of Bambachianmegaguilds, a major shift in soft substrate shelf palaeocommunities from brachiopod-dominated (in themiddle and late Palaeozoic) to bivalve-dominated, and amajor restriction in metazoan carbonate build-ups (seealso Section 4.2.1). Changes at the third level includereductions in epifaunal and infaunal tiering (see Sections4.1.4 and 4.2.1), which occurred together with numeroussmall-scale fourth-level changes.

From the evidence outlined above, a temporal struc-ture for the end-Permian mass extinction recovery inter-

2.3 Macroevolution 205

val includes: (1) the mass extinction, which ended at thebeginning of the Triassic; (2) the survival or lag, whichlasted through the Griesbachian, and, depending upongeographical location, into some or all of the Nam-malian; (3) the rebound, which probably began at differ-ent locations during various times in the Nammalian,indicated by the reappearance of gastropod Lazarustaxa, articulate crinoids, and other taxa in benthicpalaeocommunities (e.g. Schubert and Bottjer 1995;Erwin and Pan in Hart 1996; Hallam and Wignall 1997;Wignall et al. 1998; Twitchett 1999); and (4) the expansion, which began with the start of the Middle Triassic.

Thus, a variety of features, such as the presence ofopportunists, characterize the survival or lag, and thetiming of the rebound seems to have differed dependingupon geographical location. Still not resolved is why this recovery had such an unusually long duration.However, many studies of this recovery interval havefocused on the effects of continued environmental stresslinked to the cause of the mass extinction itself, such asanoxia or hypercapnia (e.g. Twitchett 1999; Woods et al.1999). Most likely this prolonged biotic recovery fromthe end-Permian mass extinction was caused by thebiotic effects of the mass extinction as well as harsh envi-ronmental conditions, both of which varied geographi-cally and temporally in the Early Triassic (e.g. Woods et al. 1999).

Conclusions

The analysis of biotic recovery from mass extinctionsprovides fascinating glimpses of how the Earth’s biotaresponds to severe stress. Taxonomic data have allowedthe recognition and an initial understanding of theserecovery intervals. Clearly, the detailed collection ofpalaeoecological data, in conjunction with additionaltaxonomic data, is needed to move the analysis of eachPhanerozoic recovery interval forward. Our goal shouldbe a general understanding of the biotic properties ofthese crisis intervals, with the ultimate aim of providingstrategies to help manage the current biodiversity crisis.

References

Bottjer, D.J. (1998) Phanerozoic non-actualistic paleoecology.Geobios 30, 885–893.

Boucot, A.J. (1983) Does evolution take place in an ecologicalvacuum? II. Journal of Paleontology 57, 1–30.

Hallam, A. and Wignall, P.B. (1997) Mass extinctions and theiraftermath. Oxford University Press, Oxford.

Hansen, T.A. (1988) Early Tertiary radiation of marine molluscsand the long-term effects of the Cretaceous–Tertiary extinc-tion. Paleobiology 14, 37–51.

Hart, M.B., ed. (1996) Biotic recovery from mass extinction events.Geological Society Special Publication no. 102.

Jablonski, D. (1986) Causes and consequences of mass extinc-tions: a comparative approach. In: D.K. Elliott, ed. Dynamicsof extinction, pp. 183–230. John Wiley and Sons, New York.

Schubert, J.K. and Bottjer, D.J. (1992) Early Triassic stromato-lites as post-mass extinction disaster forms. Geology 20,883–886.

Schubert, J.K. and Bottjer, D.J. (1995) Aftermath of thePermian–Triassic mass extinction event: paleoecology ofLower Triassic carbonates in the western USA. Palaeogeo-graphy, Palaeoclimatology, Palaeoecology 116, 1–39.

Sheehan, P.M. (1996) A new look at Ecologic Evolutionary Units(EEUs). Palaeogeography, Palaeoclimatology, Palaeoecology 127,21–32.

Twitchett, R.J. (1999) Palaeoenvironments and faunal recoveryafter the end-Permian mass extinction. Palaeogeography,Palaeoclimatology, Palaeoecology 154, 27–37.

Wignall, P.B., Morante, R. and Newton, R. (1998) The Permo-Triassic transition in Spitsbergen: d13Corg chemostratigraphy,Fe and S geochemistry, facies, fauna and trace fossils. Geologi-cal Magazine 135, 47–62.

Woods, A.D., Bottjer, D.J., Mutti, M. and Morrison, J. (1999)Lower Triassic large sea floor carbonate cements: their originand a mechanism for the prolonged biotic recovery from theend-Permian mass extinction. Geology 27, 645–648.

2.3.11 Evolutionary Trends

D.W. McSHEA

Introduction

The increase in mean body size in horses from theEocene to the Recent is an evolutionary trend. Underly-ing this trend was a particular ‘dynamic’, a tendency forsize to increase rather than decrease in all or most equidlineages; in other words, a bias in the direction of sizechange (MacFadden 1986; McShea 1994). The distinctionhere is between a pattern, the trend in the mean, and itsdynamic, or what might be called the rules of change inlineages that account for the pattern. In principle, thebody-size trend could have been produced by a differentdynamic. For example, if horses had originated at ornear a size minimum — perhaps a lower limit on sizeimposed by selection — then as the group diversified,mean size would only have increased. The dynamic isdifferent in that it involves only a local bias; that is,among the very smallest species (at their lower limit), nodecreases occur, but at larger sizes, increases anddecreases are equally frequent.

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