Comparative Evolutionary Palaeoecology: Assessing the Changing Ecology of the Past

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Comparative evolutionary palaeoecology: assessing the changing ecology of the past

DAVID J. BOTTJER, 1 JENNIFER K. SCHUBERT 2 & MARY L. DROSER 3 1Department of Earth Sciences, University of Southern California, Los Angeles, CA 90089, USA 2Department of Geological Sciences, University of Miami, Miami, FL 33124, USA 3Department of Earth Sciences, University of California, Riverside, CJl 92521, USA

Abstract: Various palaeoecological trends have been identified in the Phanerozoic, each focusing on different aspects of the fossil record. Patterns that have been described include histories of tiering, palaeocommunity species richness, and guild occupation in evolutionary faunas, as well as onshore-offshore trends in origination, expansion and retreat. Patterns of change through time have also been documented from biosedimentological features (ichnofabrics, microbial structures, shell beds). Such trends can be compared and contrasted to yield unique insights into understanding the changing ecology of the past, and in particular may be helpful in evaluating the relative degree of ecological degradation caused by a mass extinction. This comparative approach can also shed light on a variety of fundamental palaeobiological problems, for example, why no new body plans (phyla) have evolved since the early Phanerozoic. Causes of this phenomenon are thought to be either: (1) ecospace was not sufficiently open after the early Phanerozoic for survival of new body plans; or (2) accumulating developmental constraints after the early Phanerozoic have prevented the evolution of new body plans. Because the Permian-Triassic mass extinction was the most devastating biotic crisis of the Phanerozoic, one might expect new body plans to appear if ecospace were the primary limiting factor and opened sufficiently by this mass extinction. Although previous studies have shown that ecospace availability in the Cambrian and Early Triassic was indeed different, this comparative approach indicates that ecological conditions in the Early Triassic were most like those of the Late Cambrian/Early Ordovician. Thus, if ecospace availability has constrained the survival of new body plans, then ecospace has always been sufficiently filled after the Cambrian explosion to inhibit their evolution.

Evolutionary palaeoecology examines the inter- for deciphering the ecological context of mass play of evolution and ecology on a geological extinction aftermaths. time scale through the filter of the fossil and stratigraphic record. Although a variety of Phanerozoic palaeoecological trends approaches has been utilized in previous studies concerning evolutionary palaeoecology, perhaps Palaeoecology originally developed as a metho- the most significant achievement of this research dology for palaeoenvironmental reconstruction has been the recognition of long-term palaeo- (e.g. Bottjer et al. 1995). Widespread application ecological trends over 10 6 to 10 9 years. Such of ecological approaches in palaeontological trends include changes in Phanerozoic benthic data collection through the 1960s and 1970s marine palaeocommunity species richness, tier- (e.g. Valentine 1973) led to the development of a ing and evolutionary fauna guild occupation as suitably large database to facilitate syntheses of well as onshore--offshore patterns and changes long-term ecological trends through some or all through time of biosedimentological features of the Phanerozoic. Perhaps the earliest Phaner- (ichnofabrics, microbial structures, shell beds). ozoic trend to be documented was that of These trends can be compared and contrasted palaeocommunity species richness (Bambach among themselves and with other biotic trends 1977). Application of ecological approaches (such as Phanerozoic familial diversity, e.g. towards an understanding of the Precambrian Sepkoski 1992) to yield unique insight in under- fossil records has also been fruitful, with perhaps standing the changing ecology of the past. In the most convincing Precambrian palaeoecolo- particular, comparative evolutionary palaeo- gical trend being that of long-term stromatolite ecology can be an especially effective approach decline, which began in the late Proterozoic (e.g.

From Hart, M. B. (ed.), 1996, Biotic Recoveryfrom Mass Extinction Events, Geological Society Special Publication No. 102, pp. 1-13 Downloaded from http://sp.lyellcollection.org/ by guest on September 27, 2021

2 D.J. BOTTJER ET AL.

(a) (b) CAMBRIAN FAUNA MEDIAN HIGH VARIABLE OPEN NUMBER STRESS NEARSHORE MARINE OF SPECIES ENVIRONMENTS ENVIRONMENTS ENVIRONMENTS PELAGIC

CENOZOIC $.S 39 61.5 SUSPENSION HERBIVORE CARNIVORE MESOZOIC 7.5 17 2 S f UPPER II 16 30 PALEOZOIC EPIFAUNA MIDDLE 9.5 19.5 30.S SUSPENSION DEPOSIT HERBIVORE PALEOZOIC

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PELAGIC INFAUNA SUSPENSION HERBIVORE CARNIVORE SUSPENSION DEPOEIT CARNIVORE

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SHALLOW 2 4 2 EPIFAUNA DEEP SUSPENSION DEPOSIT HERBIVORE CARNIVORE

DEEP MOBILE 2 2 5

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ArrACHED 6 Fig. 1. Trends in Phanerozoic benthic marine palaeo- ERECT community species richness and evolutionary fauna guild occupation. (a) Median number of species in RECLINING 4 palaeocommunities for various Phanerozoic times and environments, modified from Bambach (1977). Ca) INFAUNA General adaptive strategies that typify the more SUSPENIION DEPOEIT CARNIVORE

diverse classes of the Cambrian evolutionary fauna. SHALLOW 3 1 1 (¢) General adaptive strategies that typify the more diverse classes of the Palaeozoic evolutionary fauna. SHALLOW 3 4 3 ACT1VE (d) General adaptive strategies that typify the more ¢.~,.:.-., ::~;....;:,:::.:,.... :...:..::: • ..-:...:::::;:-. diverse classes of the Mesozoic-Cenozoic (Modem) DEEP ':..:-v~~..:i';:::..',:.:"., 'J :.:,;:'!. :.:':-~:~.:-::."::." ";'::: evolutionary fauna. For b, c, d the number of more PASSIVE ]~.-,Y.?-:Z--"..':."":'.;.'.';:i:'.':.'::: ".." :;";-." '.': diverse classes which show each adaptive strategy is DEEP 2 1 indicated in the boxes, with empty boxes indicating no ACTIVE classes present at that time and stippled boxes indicating not biologically practical adaptive strategies; modified from Bambach (1983), identity of summed classes can be found in Bambach (1983). Downloaded from http://sp.lyellcollection.org/ by guest on September 27, 2021

COMPARATIVE EVOLUTIONARY PALAEOECOLOGY 3

Garrett 1970; Awramik 1971, 1990, 1991; Walter exploitation of more ecospace than was typical & Heys 1985). To illustrate the variety of ways in of the preceding fauna. which palaeoecological trends are documented, several examples are described below. A detailed Tiering summation of some of these as well as a variety of other palaeoecological trends can be found in Ausich & Bottjer (1982) defined tiering as the Bambach (1986), Vermeij (1987) and Sepkoski et distribution of benthic organisms within the al. (1991). space above and below the seafloor. In ecological studies the term 'stratification' is used, but Palaeocommunity species richness because this term has other meanings in geology, tiering has received widespread acceptance in Bambach (1977) synthesized data on species analyses of palaeocommunities (e.g. Watkins richness from 366 Phanerozoic palaeocommu- 1991) as well as trace fossils (e.g. Droser & nities occurring in a variety of level-bottom Bottjer 1993). Ausich & Bottjer (1982) proposed marine benthic palaeoenvironments. From this a Phanerozoic history for tiering of suspension he determined the median number of species/ feeders in level-bottom settings of one broad palaeocommunity for five Phanerozoic time palaeoenvironment, that of shallow subtidal intervals. Throughout the Phanerozoic the med- shelves and epicontinental seas. This history ian number of species always increases from has been modified in subsequent publications as marginal marine high stress environments to additional data on tiering have accumulated offshore open marine environments (Fig. l a). (Bottjer & Ausich 1986; Ausich & Bottjer 1991) Both variable nearshore and open marine (Fig. 2a). From this analysis a four-phase tiering environments show an increase in the median history can be recognized. The initial phase, number of species from the lower to the middle during the Cambrian, had very low levels of Palaeozoic, but these values then stay relatively both infaunal and epifaunal tiering (Fig. 2a). the same until the Cenozoic, when the median Phase two, from the Ordovician through the number of species/palaeocommunity for each of Permian, is characterized by complex epifaunal these environments more than doubles corre- tiering as well as, towards the end of the sponding Mesozoic values (Fig. 1a). The median Palaeozoic, increases in infaunal tiering (Fig. number of species/palaeocommunity stays about 2a). The mid-Triassic through Jurassic constitu- the same throughout the Phanerozoic in high tes phase three, and was a time where the stress marginal marine environments (Fig. l a). potential existed for maximum infaunal and This analysis was the first to show that within- epifaunal tiering (Fig. 2a). Phase four (Creta- habitat species richness has increased through ceous to present) has been a time dominated by the Phanerozoic. infaunal tiering (Fig. 2a). These changes in tiering structure are interpreted as due to a Evolutionary fauna guild occupation variety of processes, such as increased ecospace utilization, the effects of mass extinctions, and Bambach (1983) synthesized the adaptive stra- increased biotic interactions (Bottjer & Ausich tegies of major classes comprising Sepkoski's 1986; Ausich & Bottjer 1991). (1981) three great Phanerozoic evolutionary faunas (Fig. l b-d), to document changes in Onshore-offshore patterns guild occupation and hence ecospace utilization through time. The ecospace parameters consid- Shifts in habitat occupation through time, in an ered by Bambach (1983) for a broad definition onshore to offshore direction, of benthic marine of guilds are mode of life and feeding type (Fig. invertebrates were first documented by Sepkoski l b-d). Cambrian faunas utilized relatively little & Sheehan (1983) for the Cambrian/Ordovician ecospace, occupying mostly epifaunal guilds and Jablonski & Bottjer (1983) for the post- (Fig. lb). The Palaeozoic fauna shows increased Palaeozoic. Such onshore--offshore trends have occupation of epifaunal modes of life, with since been documented for assemblages of taxa diversification also into infaunal and pelagic throughout the Palaeozoic (e.g. Sepkoski & guilds (Fig. lc). The Mesozoic-Cenozoic (Mod- Miller 1985), individual clades of body fossils em) fauna is characterized by increased diversi- (e.g. Bottjer & Jablonski 1988; Jablonski & fication into infaunal guilds, as well as an Bottjer 1991; Sepkoski; 1992) (Fig. 2b), as well increase in carnivores, when compared with the as trace fossil genera (Bottjer et al. 1988). preceding faunas (Fig. ld). Bambach (1983) Onshore origination in nearshore or inner-shelf concluded from this analysis that each succeed- settings can typically be followed by two other ing evolutionary fauna was characterized by environmental patterns, expansion and retreat Downloaded from http://sp.lyellcollection.org/ by guest on September 27, 2021

4 D.J. BOTTJER ET AL.

(a) ALEozo i Esozocl 10<2 I 1o0 /,, ----,• ,m,~ • • ~- ,% ;

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~ -50 -50

-ioo 10(2

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Fig. 2. Tiering and onshore-offshore patterns. (a) Four-phase history of Phanerozoie tiering in soft substrata suspension-feeding palaeocommunities. The heaviest lines indicate the maximum infaunal and epifaunal tiering levels at any time. Other lines represent tier subdivisions. Solid fines represent data and dotted lines are inferred. From Ausich & Bottjer (1991). Co) Time-environment diagram of isocrinid crinoid presence-absence. Black boxes indicate presence of isocrinids in an assemblage of that age and environment; blank boxes indicate no data yet found for that age and environment; stippled boxes indicate presence of one or more taphonomie control taxa but absence of isocrinids in an assemblage of that age and environment. Taphonomic control taxa and palaeoenvironments are defined in Bottjer & Jablonski (1988); references for each data point are in Bottjer & Jablonski (1988); from Bottjer & Jablonski (1988). Note that Mesozoic decline in epifaunal tiering shows general correspondence with onshore--offshore retreat of isocrinid crinoids• Downloaded from http://sp.lyellcollection.org/ by guest on September 27, 2021

COMPARATIVE EVOLUTIONARY PALAEOECOLOGY 5

(Bottjer & Jablonski 1988). Expansion is defined (a) as origination onshore with later movement offshore, while retaining representatives onshore. Retreat is movement offshore with loss of onshore representatives. As an example, the pattern documented for isocrinid crinoids shows expansion in the Triassic and Jurassic, and retreat in the Late Cretaceous and Tertiary (Fig. 2b). A variety of mechanisms that might account for these long-term onshore-offshore trends has been proposed (e.g. Bottjer & Jablonski 1988; Sepkoski 1991); they do not correspond with any large-scale physical trends, PTLC TBLC MC UC LO ME) uo such as sea-level changes, and no consensus on CAMBRIAN ORDOVICIAN which biological processes lead to this intriguing AGE pattern currently exists. (b) lchnofabrics 40 Sedimentary rock fabric resulting from biotur- o bation has been termed ichnofabric (Ekdale & t; Bromley 1983). Ichnofabric includes discrete 30 Q'e) identifiable trace fossils as well as mottled 0= bedding, all produced through the activities of organisms forming surface traces and trails and 20 infaunal burrows (and borings). One approach to studying ichnofabric emphasizes determina- 10, tion of the extent or amount of bioturbation 6 recorded in a sedimentary rock. The ichnofabric z index method is a semi-quantitative approach for estimating the extent of bioturbation re- C O S D C P corded in a sedimentary rock (Droser & Bottjer AGE 1986) (Fig. 3a). Using this method, ichnofabric Fig. 3. Trends in ichnofabrics. (a) Average ichnofabric index data were recorded from Cambrian and index for carbonate inner shelf palaeoenvironments for Ordovician carbonate strata of the western Cambrian and Ordovician strata of the Great Basin in United States, in order to determine the nature western North America. PTLC, pre-trilobite Lower of the metazoan radiation into the infaunal Cambrian; TBLC, trilobite-bearing Lower Cambrian. habitat (Droser & Bottjer 1988, 1989). From this Modified from Droser & Bottjer (1993). Ca) Distribu- data an average ichnofabric index for carbonate tion of Skolithos piperock ichnofabric through the Palaeozoic. Histogram represents the number of inner shelf paleoenvironments was computed piperock occurrences as a function of age, normalized (Droser & Bottjer 1989) (Fig. 3a). This average to correct for differences in map area and duration ichnofabric index trend shows a large increase in such that the area and duration of the Cambrian is set bioturbation within the Lower Cambrian and a equal to 1. Data source listed in Droser (1991); second major increase between the Middle and modifed from Droser (1991). Upper Ordovician (Fig. 3a). Droser & Bottjer (1989) interpreted this trend in average ichno- clastic setting is characterized, particularly in fabric index as indicating, for inner-shelf palaeo- the Palaeozoic, by the presence of the trace environments, increased utilization of infaunal fossil Skolithos, which forms as a vertical tube ecospace during the early Palaeozoic. of variable length. Dense accumulations of In the same way that sedimentary facies occur Skolithos produce a characteristic ichnofabric, in strata of different ages and from different commonly termed 'piperock' (e.g. Droser 1991). geographical regions, ichnofabrics, which are Droser (1991) has compiled occurrences of types of biogenic sedimentary fabrics, also recur piperock throughout the Palaeozoic, which are (e.g. Droser 1991; Droser & Bottjer 1993). defined as densely packed Skolithos which show Because ichnofabrics are produced by biological an ichnofabric index of 3 or greater (Fig. 3b). processes, the temporal or stratigraphic distribu- This analysis shows that Skolithos piperock tion of a given ichnofabric is controlled to some occurs most abundantly in the Cambrian, extent by evolution. The nearshore terrigenous and then decreases in occurrence through the Downloaded from http://sp.lyellcollection.org/ by guest on September 27, 2021

6 D.J. BOTTJER ET AL. remainder of the Palaeozoic (Fig. 3b). Droser and environmental distribution of shell-produ- (1991) has attributed this post-Cambrian decline cers and of organisms that interact with skeletal in occurrence of piperock to two possible causes: hardparts. Two different modes of shell concen- (1) the consequences of the Ordovician faunal trations (archaic v. modern mode) were recog- radiation, when bioturbation increased in other nized by Kidwell (1990) using features such as environments and, thus, may reflect the appear- physical dimension, taxonomic composition and ance of a new and better adapted fauna in the taphonomic attributes of the shell beds. The nearshore terrigenous elastic setting; and (2) a archaic mode of shell beds is represented in systematic decrease in (preserved) shallow mar- Palaeozoic and Triassic strata and characterized ine sandstones in the post-Cambrian Palaeozoic. by relatively thin concentrations dominated by brachiopods and other epifaunal and semi- Microbial structures infaunal organisms (excepting crinoidal calcar- enites). In contrast, the modern mode is pri- Stromatolites first appeared in the Archaean, marily in Cretaceous and Cenozoic strata and became increasingly abundant and diverse in the characterized by thin pavements plus full three- Early Proterozoic, and by the Late Proterozoic dimensional bioclastic concentrations domi- had attained their maximum abundance and nated by molluscs and other epifaunal and fully diversity (Awramik 1971, 1990, 1991) (Fig. 4a). infaunal organisms (Kidwell 1990). Li & Droser However, during the latest Proterozoic, stroma- (1992) further recognized distinct differences tolites declined precipitously in diversity and between Cambrian and Ordovician shell beds. abundance (Fig. 4a), most likely owing to effects These differences reflect the dominance of the of the early diversification of metazoans (e.g. Cambrian and Palaeozoic faunas respectively. Garrett 1970; Awramik 1971, 1990, 1991), such Cambrian shell beds are dominated by trilobites as increased grazing and sediment disturbance. and occur as thin pavements whereas the archaic Stromatolites from normal marine palaeoenvir- mode described by Kidwell (1990) first really onments were still somewhat common in the occurs in the stratigraphic record in the Ordo- Cambrian and Early Ordovician, but from the vician with the appearance of the Ordovician Middle Ordovician through the remainder of the fauna and the diversification of the articulate Phanerozoic, stromatolites typically formed in brachiopods. Thus, changes in the temporal and environments characterized by hypersalinity or environmental distribution of shell beds can be hyposalinity and strong currents or wave action, directly linked to the types and ecologies of the which typically reduced activity of epifaunal, organisms living at the time. Future work (e.g. grazing and/or burrowing animals (Awramik Kidwell 1993) on shell beds will help refine 1990). This second phase of stromatolite decline Kidwell's (1990) model and indeed, it may be is attributed to the effects in marine environ- possible to recognize mass extinction events and ments of the Ordovician radiation of metazoans subsequent radiations in the shell bed record. (Awramik 1990, 1991), including increased space competition for substrates favourable for colo- Comparative evolutionary palaeoecology nization, and accelerated generation and deposi- tion of carbonate sediment (in the form of These palaeoecological trends can be compared skeletal debris and silt- and sand-sized bioclasts and contrasted with each other to yield unique and pellets) that would bury microbial mats (e.g. insights into understanding the changing ecology Pratt 1982). of the past. Such trends can also be compared with other biotic trends, such as the history of Shell beds marine familial diversity developed by Sepkoski (1981, 1992). For example, Ausich & Bottjer Shell concentrations or shell beds (any relatively (1985) postulated that there was a correlation dense accumulation of biomineralized remains between the amount of characteristic tiering with various amounts of sedimentary matrix, present (Fig. 2a) and global marine familial irrespective of taxonomic composition and diversity (as determined by Sepkoski 1981). For degree of post-mortem modification) are a suspension-feeders, this relationship holds true conspicuous and significant part of the Phaner- for the Palaeozoic, with the pattern of low ozoic stratigraphic record (KidweU 1990, 1991; epifaunal tiering in the Cambrian and rising Kidwell & Bosence 1991). However, few studies epifaunal tiering in the Ordovician, stabilizing have examined temporal patterns and trends in through the remainder of the Palaeozoic, almost shell beds. Kidwell (1990) predicted that patterns mirroring changes in marine familial diversity of shell accumulations should vary over Phaner- (Ausich & Bottjer 1985). However, amount of ozoic time because of changes in the diversity tiering and overall familial diversity are de- Downloaded from http://sp.lyellcollection.org/ by guest on September 27, 2021

COMPARATIVE EVOLUTIONARY PALAEOECOLOGY 7 coupled after the Palaeozoic (Ausich & Bottjer number occurring in the Early Triassic. This 1985). Ausich & Bottjer (1985) postulated that compilation has been expanded with newly this decoupling of diversity from tiering, parti- published data, and still shows a similar pattern cularly in the Cenozoic, may have been due to but with an even greater number of Early increased biogeographical provinciality during Triassic occurrences (Fig. 4b). Although the that time, which could have been the primary number of occurrences of normal marine stro- mechanism driving Cenozoic diversity increase. matolites documented from the literature is It is also possible that post-Palaeozoic diversity small, their relative prominence in the Early increase, not driven by increases in tiering, could Triassic (Fig. 4b) is suggestive of a real have been at least partially influenced by the phenomenon. It appears that the abundance of increase in mobile carnivores during the Meso- stromatolites in the Early Triassic, although by zoic-Cenozoic (Bambach 1983) (Fig. lb-d), no means as widespread as in the latest which would be less likely to live in a tiered Proterozoic (Fig. 4a, b), may more closely structure. approximate that of the Late Cambrian/Early Most previous applications of comparative Ordovician (Fig. 4a). This increase of normal- evolutionary palaeoecology have focused on the marine level-bottom stromatolites in the Early early metazoan radiation and increases in Triassic may be because metazoan-imposed palaeoecological complexity (e.g. Ausich & barriers to the nearshore normal-marine envir- Bottjer 1985; Allison & Briggs 1993). An onments previously dominated by stromatolites examination of the effects of mass extinctions were removed, so that opportunities for stroma- on the features documented in long-term palaeo- tolites to form in such settings were increased ecological trends, in order to understand better (Schubert & Bottjer 1992a). the causes and consequences of mass extinctions, It has long been known that Early Triassic is also an effective application of comparative macroinvertebrate assemblages characteristically evolutionary palaeoecology. Palaeoecological have a low species richness (e.g. Hallam 1991; data can be collected from fossils and strata of Erwin 1993). Only one study of Early Triassic the mass extinction aftermath. These can be used palaeocommunity structure has been done, from to gauge the type and degree of ecological Lower Triassic (Nammalian, Spathian) carbo- degradation caused by the mass extinction, by nate strata in western North America, deposited determining if aftermath ecological indicators in shelfal settings, where 8 palaeocommunities resemble those of any earlier time periods were identified (Schubert 1993; Schubert & documented in the long-term trends. Results Bottjer 1995). The number of samples which from this comparative analysis might indicate define these palaeocommunities is low, so that a that all ecological parameters show degradation statistical comparison of species richness is not to a single earlier time interval, or to several possible. However, the average number of different time intervals. species in collections defining these palaeocommunities is 13 (Schubert 1993; Schubert & Permian-Triassic mass extinction aftermath Bottjer 1995). Using Bambaeh's (1977) environmental classification (Fig. l a), these Early The Permian-Triassic mass extinction is the Triassic palaeo-communities would have been greatest of all Phanerozoic mass extinctions living in either variable nearshore environments (e.g. Raup 1979; Sepkoski 1992). Recent studies or open marine environments. Comparison with indicate that the aftermath of this mass extinc- Bambach's (1977) raw data and determination tion lasted through the Early Triassic (e.g. of median palaeocommunity species richness Hallam 1991, 1995; Schubert 1993; Schubert & (Fig. l a), as well as with data from particular Bottjer 1995), a time interval approximately Permian and later Triassic palaeocommunities 4Ma long (Harland et al. 1990). A variety of (Schubert & Bottjer 1995), indicates that species palaeoecological data has been collected from richness of these Early Triassic palaeocommu- Lower Triassic marine strata, which can be used nities is lower than typical upper Palaeozoic or to assess the ecological degradation caused by other Mesozoic palaeocommunities from similar the mass extinction. environments, and is most compatible with From an extensive literature search Schubert species richness from lower Palaeozoic palaeo- & Bottjer (1992a) compiled reported occurrences communities. of stromatolites from strata of Silurian and Ecospace was to some extent emptied by the younger ages deposited in normal-marine level- Permian-Triassic mass extinction (Erwin et al. bottom palaeoenvironments. Very few records 1987). Of the possible guilds in Bambach's of stromatolites in normal-marine level-bottom (1993) ecospace utilization analysis (Fig. 2b-d), settings were forthcoming, with the greatest only 5 are occupied in the Early Triassic Downloaded from http://sp.lyellcollection.org/ by guest on September 27, 2021

8 D.J. BOTI'JER ET AL.

PHANEROZOIC

FIRST ANIMALS

1 .O N

PROTEROZOIC

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- 440 MY - Co) TIME PERIOD Fig. 4. Trends in stromatolites. (a) Relative abundance of stromatolites plotted against time; modified from Awramik (1991). Ca) Histogram of normal-marine level-bottom stromatolites (left to right) in Silurian, Late Devonian, Mississippian, Pennsylvanian, Late Permian, Early Triassic, Late Triassic, Jurassic and Cenozoic (K, Cretaceous; Cz, Cenozoic). Data sources listed in Schubert & Bottjer (1992a) with the addition of an Early Triassic occurrence (Wignall & Hallam 1992) and a Cenozoic occurrence (Braga et al. 1995); modified from Schubert & Bottjer (1992a). Downloaded from http://sp.lyellcollection.org/ by guest on September 27, 2021

COMPARATIVE EVOLUTIONARY PALAEOECOLOGY 9 palaeocommunities documented from western bearing Lower Cambrian through Middle Or- North America (Schubert 1993; Schubert & dovician strata studied by Droser & Bottjer Bottjer 1995). Comparison with Bambach's (1988, 1989) (Fig. 3a). (1983) analysis of ecospace utilization by the Nearshore sandstones characterized by Sko- three great evolutionary faunas shows that these lithos piperock ichnofabric (e.g. Droser & Early Triassic palaeocommunities (although not Bottjer 1990) are rare in the post-Palaeozoic representing a worldwide database as is Barn- (Droser 1991). Nevertheless, the only Lower bach's (1983)) are more similar to the Cambrian Triassic nearshore sandstone that we are aware fauna, which occupies 9 of the ecospace cate- of, the Bjorne Formation in the Canadian gories, than the Palaeozoic fauna (14 ecospace Arctic, exhibits a Skolithos piperock ichnofabric categories) or the Mesozoic-Cenozoic (Modern) (Devaney 1991). Thus, ichnofabric type in this fauna (20 ecospace categories) (Fig. 2b-d). setting is a holdover from the Palaeozoic. A Erwin et al. (1987), from available Triassic data, similar Palaeozoic holdover pattern is found calculated that at least 15 ecospace categories with shell beds (Kidwell 1990). were occupied during this time period. However, This analysis indicates that ecospace occupa- by combining data from the Early Triassic with tion was diminished by the Permian-Triassic those from the Middle and Late Triassic, this mass extinction to levels characteristic of the analysis (Erwin et al. 1987), while useful for Late Cambrian/Early Ordovician. The evidence understanding the Mesozoic radiation, is very which provides the most robust support for this likely an overestimation of ecospace occupation conclusion is from stromatolite occurrence and during the Early Triassic aftermath. tiering structure. The other lines of evidence - This reduction in ecospace utilization is also palaeocommunity species richness, ecospace shown in Early Triassic patterns of tiering. Early utilization, ichnofabrics and shell beds - are in Triassic palaeocommunities, not only in western need of additional development but show every North America but worldwide, had very low indication of being compatible with this inter- levels of epifaunal tiering (Schubert & Bottjer pretation. That ecospace utilization was altered 1992b, 1995), with only the 0 to +5cm tier by the Permian-Triassic mass extinction is not a present in the earliest Early Triassic (Gries- novel conclusion (e.g. Erwin et al. 1987), but bachian, Nammalian) and the 0 to + 5 cm and demonstration that the Early Triassic had + 5 to + 20 cm tiers present in the later Early patterns of ecospace utilization similar to an Triassic (Spathian). Analysis of bioturbation in earlier time in the Phanerozoic has implications lower Triassic strata of western North America for our understanding of constraints on origina- (Bottjer et al. 1993; Schubert 1993; Schubert tion of higher taxa. & Bottjer 1995) and the southern Alps (Italy) indicates that only the 0 to -6cm and -6 to Why no new phyla after the Cambrian -12 cm tiers are present, and that this pattern explosion? may be worldwide. When compared with characteristic Phanerozoic tiering patterns (e.g. One of the most striking patterns of the fossil Bottjer & Ausich 1986; Ausich & Bottjer 1991), record is that origination of 10 to 11 phyla with these reduced levels of tiering are most like those skeletonized representatives is confined to the exhibited by Late Cambrian or Early Ordovician Vendian-Cambrian (e.g. Erwin et al. 1987; faunas (Fig. 2a). Valentine 1995), a phenomenon that is com- Systematic measurement of ichnofabric in- monly called the Cambrian explosion. This dices has yet to be done for Lower Triassic interval of phylum-level origination is basically strata. Preliminary observations indicate that all over by the end of the Middle Cambrian, with ichnofabric indices, from 1 (no preserved bio- only the Bryozoa appearing later in the Early turbation) to 5 (completely bioturbated), can be Ordovician (although this Early Ordovician found in Lower Triassic carbonate strata depos- skeletonized bryozoan could have been preceded ited in shelf palaeoenvironments of western by non-skeletonized members) (e.g. Erwin et al. North America (Schubert 1993; Schubert & 1987; Valentine 1995). The two leading mechan- Bottjer 1995) and the southern Alps (Italy). isms for the restriction of phylum-level origina- However, because bioturbation in these rocks is tion to the Cambrian attribute this pattern to either horizontal or relatively shallow, storm either of what have come to be termed the beds with relatively low amounts of bioturbation genome and ecospace hypotheses (e.g. Valentine are commonly preserved (Schubert 1993), so 1973, 1980, 1986, 1992, 1995; Erwin et aL 1987; that the preserved amount of bioturbation Valentine & Erwin 1987; Jablonski & Bottjer appears to be less like that of the Upper 1990; Erwin 1994). Ordovician and more like that of the trilobite- The ecospace hypothesis holds that the more Downloaded from http://sp.lyellcollection.org/ by guest on September 27, 2021

10 D.J. BOTTJER ET AL. open ecospace of the Vendian-Cambrian pre- utilization for the remainder of the Phanerozoic. sented an ecological setting of greater opportu- Because 15 of the 20 possible marine adaptive nity for divergent morphologies than that of types defined by Bambach (1983) were present in later times (e.g. Bambach 1983) (Fig. lb-d). As the Triassic, actually a slight increase over the these phyla became established and diversified in Palaeozoic fauna (Fig. lc), Erwin et al. (1987) different ecological roles, and as ecospace filled, concluded that survivors of the mass extinction they would competitively exclude members of represented a broad variety of body plans thinly other clades with innovations that might lead scattered among adaptive zones. Such a pattern them to similar or overlapping modes of life (e.g. or ecospace utilization could have effectively Valentine 1973, 1980, 1995; Erwin et al. 1987; served to inhibit the occurrence of phylum-level Jablonski & Bottjer 1990; Erwin 1994). A central innovations (Erwin et al. 1987). tenet of the ecological hypothesis is that evolu- However, an even more revealing test would tionary innovation, particularly at the phylum- be to determine ecospace utilization during the level, has occurred generally at constant rates Early Triassic, the genuine aftermath interval of since the appearance of the first metazoans (e.g. this mass extinction (e.g. Hallam 1991, 1995; Jablonski & Bottjer 1990). Thus, by the Late Schubert 1993) and very likely the time of least Cambrian, occupation of marine ecospace ecospace utilization during the post-Middle would have risen to the level where no innova- Cambrian. The analysis of ecospace utilization tions at the phylum-level would be successful. for this time period outlined herein indicates that The genome hypothesis as originally devel- Early Triassic ecospace was occupied at levels oped maintained that major alterations in early similar to those found in the Late Cambrian/ metazoan development were more easily attain- Early Ordovician and thus was not degraded to able because their genomes were less highly levels prevalent during the Cambrian explosion. canalized and had fewer among-gene interac- These results, in conjunction with those of Erwin tions (e.g. Valentine 1986, 1992; Valentine & et al. (1987), do not lead to conclusions as to the Erwin 1987). Later metazoans with more cana- primacy of the ecospace or genome hypotheses. lized genomes would have faced increasing Instead they support the conclusion that if developmental constraints that would not have ecospace availability has indeed constrained the allowed the generation of major innovations at survival of new phylum-level innovations, then the phylum level (e.g. Valentine 1986, 1992; ecospace has always been sufficiently filled after Jablonski & Bottjer 1990). Origin of new phyla the Cambrian explosion to inhibit their evolu- would thus have been temporally restricted to tion. As an intriguing postscript, Valentine the early phase of metazoan evolution. There- (1995) has recently concluded, through an fore, the major difference between the two analysis of the Hox/HOM homeobox genes, hypotheses is that the ecospace hypothesis that the current understanding of the molecular predicts a constant rate of phylum-level innova- basis of development provides no support for tion, while the genome hypothesis predicts a rate the genome hypothesis, and that the ecospace of appearance for such innovations that rapidly hypothesis is more consistent as an explanation declined to zero. for the concentrated origin of phyla during the A traditional test of these two hypotheses has Cambrian explosion. been to search for other times in the Phanerozoic where ecospace occupation might be reduced to Conclusions levels of the Vendian/Early-Middle Cambrian. The most appropriate time would be during a The comparative evolutionary palaeoecology mass extinction aftermath. If ecospace during approach can produce unique insights into the such a time was reduced to the levels prevalent evolutionary and ecological history of life, and during the Cambrian explosion, and yet no new the processes which have driven this history. phyla appeared, then this could be interpreted as This approach can grow through further refine- support for the genome hypothesis. ment of the long-term palaeoecological trends Because no mass extinction has been larger, that have already been identified, as well as the Permian-Triassic mass extinction aftermath continued development of new palaeoecological has been the logical place to conduct such a test trends. In particular, application of comparative (e.g. Erwin et al. 1987; Valentine 1992). Using a evolutionary palaeoecology promises to be similar but simpler approach to the comparative especially useful in allowing a better under- evolutionary palaeoecology approach outlined standing of the ecological processes operating herein, Erwin et al. (1987) evaluated ecospace during and after mass extinctions. utilization for the entire Triassic and compared Such an approach can also help to character- this with Bambach's (1983) results on ecospace ize systematically differences between the several Downloaded from http://sp.lyellcollection.org/ by guest on September 27, 2021

COMPARATIVE EVOLUTIONARY PALAEOECOLOGY 11 mass extinctions and their aftermaths. For References example, before the Frasnian-Famennian mass extinction glass sponges lived only in deeper ALLISON, P. A. & BRIGGS, D. E. G. 1993. Exceptional water regions, but during the mass extinction fossil record: Distribution of soft-tissue preserva- aftermath they are found in shallow water tion through the Phanerozoic. Geology, 21, 527- palaeoenvironments, where they underwent a 530. AUSICH, W. I. & BoTrJER, D.J. 1982. Tiering in burst of diversification (e.g. McGhee 1996). This suspension-feeding communities on soft substrata reversed onshore-offshore pattern is considered throughout the Phanerozoic. Science, 216, 173- to be a key piece of evidence for unravelling the 174. cause of the Frasnian-Famennian mass extinc- -- & -- 1985. Phanerozoic tiering in sus- tion (e.g. McGhee 1996). 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