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Decoupled evolution of soft and hard substrate communities during the and Great Biodiversification Event

Luis A. Buatoisa,1, Maria G. Mánganoa, Ricardo A. Oleab, and Mark A. Wilsonc

aDepartment of Geological Sciences, University of Saskatchewan, Saskatoon, SK, Canada S7N 5E2; bEastern Energy Resources Science Center, US Geological Survey, Reston, VA 20192; and cDepartment of , The College of Wooster, Wooster, OH 44691

Edited by Steven M. Holland, University of Georgia, Athens, GA, and accepted by Editorial Board Member David Jablonski May 6, 2016 (received for review November 21, 2015) Contrasts between the Cambrian Explosion (CE) and the Great shed light on the natures of both radiations. Because there is still Ordovician Biodiversification Event (GOBE) have long been recog- controversy regarding Sepkoski’s nonstandardized curves of nized. Whereas the vast majority of body plans were established taxonomic diversity (13–15), a rarefaction analysis as a result of the CE, taxonomic increases during the GOBE were was performed in an attempt to standardize diversity data. The manifested at lower taxonomic levels. Assessing changes of ichno- aims of this paper are to document the contrasting ichnodiversity diversity and ichnodisparity as a result of these two evolutionary and ichnodisparity trajectories in soft and hard substrate com- events may shed light on the dynamics of both radiations. The early munities during these two evolutionary events and to discuss the Cambrian ( 1 and 2) displayed a dramatic increase in ichnodi- possible underlying causes of this decoupled evolution. versity and ichnodisparity in softground communities. In contrast to this evolutionary explosion in structures, only a few Results Cambrian bioerosion structures are known. After the middle to late Figs. 1 and 2 summarize ichnodiversity and ichnodisparity changes, Cambrian diversity plateau, ichnodiversity in softground communi- respectively, from the through the Ordovician (SI Ap- ties shows a continuous increase during the Ordovician in both pendix, Tables S1 and S2). According to these data, the early EVOLUTION shallow- and deep-marine environments. This Ordovician increase in Cambrian (series 1 and 2) displayed a dramatic increase in diversity bioturbation diversity was not paralleled by an equally significant and disparity of bioturbation structures (12). Whereas a maxi- increase in ichnodisparity as it was during the CE. However, hard mum of 10 ichnogenera of bioturbation structures have been substrate communities were significantly different during the GOBE, recorded in Ediacaran strata (9 in the Vendian and 7 in the Nama with an increase in ichnodiversity and ichnodisparity. Innovations in macrobioerosion clearly lagged behind –substrate interactions subdivisions), 40 ichnogenera are known from strata, 59 from 2, 71 from stage 3, and 75 from stage 4 (Fig. 1 and in unconsolidated sediment. The underlying causes of this evolution- SI Appendix ary decoupling are unclear but may have involved three interrelated , Table S1). The rapid increase in behavioral patterns factors: (i) a Middle to Late Ordovician increase in available hard of bioturbation structures is also displayed at the scale of ichno- SI Appendix substrates for bioerosion, (ii) increased , and (iii) higher disparity (Fig. 2 and , Table S2). Specifically, there energetic requirements for bioerosion compared with bioturbation. are a maximum of 6 categories of architectural designs (5 in the Vendian and 4 in the Nama subdivisions) in Ediacaran strata in bioturbation | bioerosion | trace | evolutionary radiations | contrast to 20 in Fortunian strata (27 from stage 2, 31 from stage rarefaction analysis 3, and 32 from stage 4). The maximum increase in both ichno- diversity and ichnodisparity took place during the Fortunian, he Cambrian Explosion (CE) and the Great Ordovician Bio- Tdiversification Event (GOBE) are the two evolutionary radi- Significance ations that shaped the marine biosphere (1–7). The contrasting natures of the Cambrian and Ordovician radiations The majority of body plans were established during the Cam- have long been recognized. Body information suggests that brian Explosion (CE), whereas the significant taxonomic in- the vast majority of body plans emerged during of the CE and that creases during the Great Ordovician Biodiversification Event taxonomic increases during the GOBE took place at lower taxo- (GOBE) were manifest at lower taxonomic levels. Data on the nomic levels (8). However, there is still debate about whether diversity and disparity of bioturbation and bioerosion indicate these two events were independent or whether the GOBE was an that soft and hard substrate communities experienced decou- extension of the CE (8–10). pled evolution. Ichnofossil data indicate that rapid diversifica- Research on the nature of these two events has concentrated tion of bioturbation occurred during the early early Cambrian on body fossils. Initial research focused on shelly fossils, but later (Fortunian) rather than during the late early Cambrian as in- soft-bodied faunas were included due to the spectacular pres- dicated by shelly fossils. The first rapid increase in bioerosion ervation of -type biotas, originally reported for the took place during the GOBE approximately 80 My after the CE Cambrian and lately for the Ordovician (9, 10). In comparison, in bioturbation. information has not been used to the same degree. Significantly, ichnologic evidence is essential to evaluate how the Author contributions: L.A.B. and M.G.M. designed research; L.A.B., M.G.M., R.A.O., and M.A.W. performed research; R.A.O. contributed analytic tools; L.A.B., M.G.M., R.A.O., and interactions between organisms and substrate responded to these M.A.W. analyzed data; L.A.B. and R.A.O. wrote the SI Appendix; and L.A.B. wrote the two major evolutionary events (11, 12). Also, because trace fossils paper. essentially represent a continuous record of soft-bodied organisms, The authors declare no conflict of interest. ichnologic information provides an independent line of evidence to This article is a PNAS Direct Submission. S.M.H. is a guest editor invited by the Editorial that of shelly fossils, therefore helping to calibrate these two evo- Board. lutionary radiations (12). Assessing changes in animal–substrate 1To whom correspondence should be addressed. Email: [email protected] interactions in both soft (bioturbation) and hard (bioerosion) This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. substrate communities as a result of the CE and the GOBE may 1073/pnas.1523087113/-/DCSupplemental.

www.pnas.org/cgi/doi/10.1073/pnas.1523087113 PNAS Early Edition | 1of4 Downloaded by guest on September 26, 2021 Fig. 1. Ichnodiversity changes during the Ediacaran-Ordovician. Ichnogenera were plotted as range-through data (i.e., recording for each ichnogenus its lower and upper appearances and then extrapolating the ichnogenus presence through any intervening gap in the continuity of its record).

which displays a 300% increase in ichnodiversity and 233% in (Granulohyalichnus and Tubulohyalichnus) have their first occurrence ichnodisparity with respect to Ediacaran data. The subsequent in the Archean (22, 23). Although these ichnogenera have not more modest ichnodisparity increase in stage 2 (35% with respect been recorded in Ediacaran-Ordovician strata, they do occur in to the Fortunian) reflects in part the appearance of vertical burrows younger rocks (23) and, therefore, have been added to the list. of suspension feeders (i.e., vertical simple burrows, vertical single Granulohyalichnus has been placed in the category of globular to U- and Y-shaped burrows) and to a lesser extent of detritus feeders spherical borings. However, microborings included in Tubulohya- (i.e., vertical concentrically filled burrows) (12, 16). Ichnodisparity lichnus display a wide variety of morphologies, most likely repre- and ichnodiversity reached a plateau in stages 3 and 4, respectively, senting more than one ichnogenus. Its type ichnospecies, T. simplus, which continued during the rest of the Cambrian, suggesting that by is included within the architectural category of cylindrical vertical to the end of the early Cambrian the was nearly oblique borings, whereas the remaining ichnospecies are awaiting over (12). This pattern is remarkably consistent with that indicated taxonomic review. by the body fossil record (6, 7) and has been confirmed by rare- In contrast with CE data, a different pattern emerges from the faction analysis (SI Appendix, Rarefaction Analysis). analysis of GOBE global ichnodiversity and ichnodisparity data. Contrasting with this evolutionary explosion in bioturbation After the middle to late Cambrian plateau, diversity of bioturbation structures, Cambrian bioerosion structures are only represented structures shows a continuous increase during the Ordovician in by four categories of architectural design: circular holes, cylin- both shallow- and deep-marine environments. The Ordovician in- drical vertical to oblique borings, fracture-shaped borings, and glob- crease in diversity is expressed in both raw and rarified data ular to spherical borings. Oichnus, Trypanites,andMandibulichnus are (SI Appendix, Rarefaction Analysis). However, rarefaction analysis knownfromCambrianstrata(17–20), the former being already demonstrates that the middle to late Cambrian diversity plateau for present in Ediacaran strata (21). Two microbioerosion ichnogenera deep-marine environments is simply an artifact resulting from lack

Fig. 2. Ichnodisparity changes during the Ediacaran-Ordovician. Categories of architectural design were plotted as range-through data (i.e., recording for each category its lower and upper appearances and then extrapolating the presence of each category through any intervening gap in the continuity of its record).

2of4 | www.pnas.org/cgi/doi/10.1073/pnas.1523087113 Buatois et al. Downloaded by guest on September 26, 2021 of data. The data compilations indicate that diversity of Ordovician an artifact related with sampling size and that fluctuations in the bioturbation structures showed a 46% increase from the Trem- diversity of bioturbation structures that may have occurred during adocian (72 ichnogenera) to the (105 ichnogenera) in the middle Cambrian to . shallow-marine environments and a 77% increase (31 ichnogenera In addition, the data reveal that the contrasting natures of the in the to 55 ichnogenera in the Hirnantian) in deep- CE and the GOBE are expressed not only by body fossils but also marine environments (Fig. 1 and SI Appendix,TableS1). In contrast by trace fossils. Analysis of the body fossil record indicates that to the trends during the CE, this Ordovician increase in diversity of the overwhelming majority of body plans emerged during the CE bioturbation structures is not paralleled by an equally significant and that taxonomic increases during the GOBE occurred at increase in ichnodisparity (21% with respect to Cambrian levels). If lower taxonomic levels (8). The fossil record of bioturbation both shallow- and deep-marine ichnodisparity are plotted sepa- mimics this pattern. Whereas the CE data show a rapid increase rately, then it is clear that the increase in ichnodisparity for the most of both diversity and disparity of bioturbation structures, the part took place in deep-marine settings and that ichnodisparity in GOBE data display a remarkable increase in diversity of bio- shallow-marine settings was similar during both the Cambrian and turbation structures, which is not paralleled by an equally signifi- Ordovician. Because a significant number of the architectural cat- cant increase in ichnodisparity. In fact, Ordovician shallow-marine egories that characterize Ordovician deep-sea settings first occurred show disparity levels of bioturbation structures that are in shallow-marine settings during the Cambrian and later migrated very similar to those in the Cambrian. This pattern is similar to that to the deep sea, the taxonomic innovations taking place in the deep noted with body fossils, revealing a rapid disparity increase that sea were probably limited, therefore resulting in a minor increase in exceeds initial diversification, therefore implying early large steps global ichnodisparity. Incidentally, data analysis provides robust in disparity and smaller ones subsequently (28–30). “ ” support for the onshore-offshore model, which invokes onshore This study points to contrasting ichnodiversity and ichnodis- origination of evolutionary innovations and their subsequent ex- parity trajectories in soft and hard substrate communities during pansion to deeper water (24, 25). the CE and GOBE. Innovations in bioerosion clearly lagged In contrast with bioturbation, the historical pattern for bio- behind animal–substrate interactions in unconsolidated sediment. erosion structures is significantly different, with an increase not Data compilations show that the rapid increase in bioerosion took only in ichnodiversity but also in ichnodisparity during the Or- ∼ Gastrochaenolites Podichnus place 80 My after the Cambrian explosion in bioturbation. The dovician. Two ichnogenera ( and ) underlying causes of this decoupling between bioerosion and were added during the Early Ordovician and two more (Cae- dichnus Tremichnus bioturbation are unclear, but three interrelated factors may have EVOLUTION and ) during the Middle Ordovician. Raw been involved. First, it is possible there was a Middle to Late data indicate that the abrupt increase in diversity of bioerosion Ordovician increase in available hard substrates for bioerosion, structures, however, took place during the Late Ordovician with which would have increased ecospace for boring . Al- the addition of 16 new ichnogenera to reach a total of 25 ich- though may have been locally common nogenera by the end of the Ordovician (178% increase). This during the Early Ordovician (31), they increased in global abun- large change is also displayed by ichnodisparity data (Fig. 2 and SI dance later during the Ordovician (32, 33). However, the recent Appendix,TableS2), with 6 categories of architectural design being discovery of Cambrian series 3 nonbioeroded hardgrounds sug- present during the Early and Middle Ordovician vs. 14 during the gests that substrates were available for potential macroborers in at Late Ordovician (133% increase). Therefore, the systematic anal- least some settings (34). In any case, the absence of bioerosion in ysis of raw ichnodiversity data clearly supports the notion of an these hardgrounds may be taken as further evidence of the mac- Ordovician bioerosion revolution (26). Rarefaction analysis based on actual counting of specimens of bioerosion structures (SI Ap- roevolutionary lag displayed by hard substrate communities. Shelly pendix, Rarefaction Analysis) also supports this marked increase substrates appear to have become more common from the Middle in diversity. to Late Ordovician (35, 36), but detailed stage-by-stage data are lacking. Second, whereas the trend toward infaunalization in un- Discussion consolidated substrates started well before a marked increase in Notably, the ichnodiversity curve (Fig. 1) is strikingly similar to predation pressures (37), the penetration of infaunal organisms that of Phanerozoic diversity curves of marine animal genera into hard substrates during the GOBE may have been driven by (27). Both trace fossil and shelly fossil genera show an explosive increased predation. The endolithic realm may have served as a diversification during the early Cambrian and more continuous refugium from predation, likely even safer than the infaunal diversification during the Ordovician. As with the curves showing habitat (38). At the same time, some bioerosion structures them- Oichnus marine animal diversity during the early Paleozoic (1), bio- selves (e.g., ) were produced by predators, therefore turbation diversity supports a two-phase kinetic model of logistic resulting in feedback loops promoting further penetration in hard diversification, corresponding to the CE and the GOBE. Each substrates. Third, in most cases, the energy involved in penetrating phase is characterized by an initial lag stage, followed by a growth hard substrates is greater than that involved in disturbing un- stage, and culminating in an equilibrium stage. This pattern sug- consolidated sediment. Modern ecologic work on this topic gests common trends in shelly and soft-bodied organisms, there- is sparse, although it is reasonable to infer that the mechanical fore reinforcing the notion of overarching evolutionary radiations grinding of a cemented substrate is a much more energetic process rather than taphonomic or sampling artifacts. than burrowing in unconsolidated sediment. An energy-based Two main departures with respect to curves based on body explanation is consistent with the fact that bioerosion in conti- fossils are noted. First, ichnologic evidence indicates that rapid nental environments also experienced a significant macroevolu- diversification took place during the early early Cambrian (12) tionary lag with respect to bioturbation in similar settings (39). rather than during the late early Cambrian as indicated by shelly Finally, the present study shows that increases in ichnodiver- fossils. Accordingly, the early early Cambrian (Fortunian) may sity are invariably linked to evolutionary radiations but are not be regarded as part of a phylogenetic fuse, pushing the earliest necessarily sufficient conditions for an increase in ichnodisparity. fossil record of most of the main body plans back in time close to The CE and GOBE data suggest that the key factor in ichno- the Ediacaran-Cambrian boundary (12). Second, whereas marine disparity construction is the exploitation of empty or underused animal genera show minor diversity fluctuations during the ecospace (39). In the present case, this conclusion is supported middle to late Cambrian, raw data show that trace fossil diversity by the fact that the CE and GOBE instances of remarkable ich- reached a plateau at the beginning of the GOBE. However, nodisparity increases were clearly linked to colonization of new rarefied diversity data show that this pre-GOBE plateau may be ecospace, namely the overall increase in disparity of bioturbation

Buatois et al. PNAS Early Edition | 3of4 Downloaded by guest on September 26, 2021 structures during the Fortunian and the overall increase in disparity Nama (41), and the 10 and 7 official stages for the Cambrian and Ordovician, of bioerosion structures during the Late Ordovician. respectively, were considered. Ichnogeneric and categories of architectural design occurrences were compiled on a case-by-case basis, thereby summarizing Materials, Methods, and Concepts actual occurrences. Ichnogenera and categories of architectural designs were plotted as “range-through” data (i.e., recording the lower and upper appear- The concepts of ichnodiversity and ichnodisparity (40) are central to the data analysis of this paper. In particular, global ichnodiversity (i.e., number ances for each ichnogenus/architectural design and then extrapolating the of ichnogenera per time slice or trace fossil richness) is used as a proxy design presence through any intervening gap in the continuity of its record) to for behavioral changes and evolutionary innovations during the CE and avoid the noise introduced by uneven sampling and availability of studies. To GOBE. In addition, the concept of ichnodisparity (i.e., number of trace fossil evaluate the effects of sample size on the diversity curves, a rarefaction analysis – architectural designs) is used to record basic morphological plans in bio- of these data were undertaken (SI Appendix,Figs.S1 S5). Because of the need genic structures (SI Appendix, Table S3). It is implied that ichnodisparity for a consistent ichnotaxonomic approach, each original taxonomic de- reveals major innovations in , locomotory , and behavioral termination was revised, and synonymies were checked. The ichnodiversity program (12). curves were compiled at the ichnogenus level because the genus taxonomy is Ichnodiversity trajectories were reconstructed using a compilation of ich- more firmly established than the species taxonomy. nogenera from the Ediacaran to the Ordovician. A previous trace fossil database encompassing the Ediacaran to lower Cambrian (12) was taken as a starting ACKNOWLEDGMENTS. Ricardo Astini, Stefan Bengtson, Jake Benner, Andrey point. This compilation is based on systematic and critical examination of the Dronov, David Jablonski, Noel James, Eduardo Mayoral, Arnie Miller, James literature, collection material, and field data. This database is here expanded Sprinkle, Steve Stanley, Leif Tapanila, and Olev Vinn provided useful feedback during the course of this project. We received valuable reviews by Thomas by the addition of middle Cambrian to Late Ordovician ichnofaunas. Bio- Servais, an anonymous referee, and the Editor. Kai Zhou assisted us with erosion and bioturbation ichnotaxa were considered separately (SI Appendix, plotting the information in tables and charts. We thank John Repetski and Chris – Tables S4 S6). The same procedure was followed for ichnodisparity by plotting Swezey for insightful comments. Financial support for this research was provided architectural designs (SI Appendix,TablesS7–S9). Data were plotted using by Natural Sciences and Engineering Research Council Discovery Grants 5-My bins. Nineteen time slices: 2 informal Ediacaran subdivisions, Vendian and 311727-05/08/13 and 311726-05/08/15 (to M.G.M. and L.A.B., respectively).

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