The other biodiversity record: Innovations in animal-substrate interactions through geologic time Luis A. Buatois, Dept. of Geological Sciences, University of Saskatchewan, 114 Science Place, Saskatoon SK S7N 5E2, Canada, luis. [email protected]; and M. Gabriela Mángano, Dept. of Geological Sciences, University of Saskatchewan, 114 Science Place, Saskatoon SK S7N 5E2, Canada, [email protected] ABSTRACT 1979; Bambach, 1977; Sepkoski, 1978, 1979, and Droser, 2004; Mángano and Buatois, Tracking biodiversity changes based on 1984, 1997). However, this has been marked 2014; Buatois et al., 2016a), rather than on body fossils through geologic time became by controversies regarding the nature of the whole Phanerozoic. In this study we diversity trajectories and their potential one of the main objectives of paleontology tackle this issue based on a systematic and biases (e.g., Sepkoski et al., 1981; Alroy, in the 1980s. Trace fossils represent an alter- global compilation of trace-fossil data 2010; Crampton et al., 2003; Holland, 2010; native record to evaluate secular changes in in the stratigraphic record. We show that Bush and Bambach, 2015). In these studies, diversity. A quantitative ichnologic analysis, quantitative ichnologic analysis indicates diversity has been invariably assessed based based on a comprehensive and global data that the three main marine evolutionary on body fossils. set, has been undertaken in order to evaluate radiations inferred from body fossils, namely Trace fossils represent an alternative temporal trends in diversity of bioturbation the Cambrian Explosion, Great Ordovician record to assess secular changes in bio- and bioerosion structures. The results of this Biodiversification Event, and Mesozoic diversity. Trace-fossil data were given less study indicate that the three main marine Marine Revolution, are also expressed in the attention and were considered briefly in evolutionary radiations (Cambrian Explo- trace-fossil record. In addition, the trace- only one of the more classic studies of bio- sion, Great Ordovician Biodiversification fossil record of continental environments diversity through time (e.g., the so-called Event, and Mesozoic Marine Revolution) suggests variable rates of increases in diversity, consensus paper by Sepkoski et al., 1981; detected in the body-fossil record are also with major radiations in the Ludlow–Early see also Mil ler, 2009). Ichnologic informa- Devonian, Cisuralian, Early Jurassic, Late expressed in the trace-fossil record. Analysis tion in the consensus paper was based on of ichnodiversity trajectories in marine Cretaceous, and Eocene, and slower increases early attempts of quantifying trace-fossil or plateaus in between these periods. environments supports Sepkoski’s logistic diversity, which were supported by the very model, which was originally based on limited data available at the time (Seilacher, CONCEPTS AND METHODS analysis of marine body fossils. The trace- 1974, 1977). The decision by Dolf Seilacher Trace fossils comprise distinctive struc- fossil record of continental environments to decline co-authorship of the consensus tures of biogenic origin, reflecting organism suggests variable rates of increases in ichno- paper reflects his doubts with respect to the diversity, with major radiations in the support that trace-fossil evidence was actu- behaviors while interacting with the Ludlow–Early Devonian, Cisuralian, Early ally providing to the diversity curves based on substrate (Fig. 1). Trace fossils may be Jurassic, Late Cretaceous, and Eocene, and body fossils. In a letter addressed to Sepkoski, preserved in a wide variety of substrates. slower increases or plateaus in between these dated 23 February 1981, Seilacher stated, Bioturbation structures occur in sediment, periods. Our study indicates that ichnologic “By lumping the two groups you may get a whereas bio- erosion structures are produced information represents an independent line curve that pleases you, but this might be an in rigid substrates, such as hardgrounds, of evidence that yields valuable insights to accident. The curve you have in mind (based clasts, bones, or rocks (Frey and Wheatcroft, evaluate paleobiologic megatrends. on the record of body fossils) is mainly one of 1989). Although the same type of trace-fossil shallow marine diversity. Including the flysch can be produced by phylogenetically INTRODUCTION (i.e., the deepwater) counts (which by their unrelated animals, in many instances trace The astounding diversity of animals in high diversity influence the results very fossils can be attributed to a producer with modern oceans and continents is the result of much), I am afraid will do no justice to the variable levels of confidence. For example, macroevolutionary processes operating in cause, although the result may fit the general the branching burrow system Ophiomorpha deep time. Conservative estimates suggest the picture” (Miller, 2009, p. 379). is commonly regarded as produced by modern biosphere hosts close to 13 million No attempts to produce global compre- decapod crustaceans, typically callianassids species, of which approximately only 4% hensive compilations have been done since (Fig. 1) (Frey et al., 1978). However, such are marine (Benton, 2001). Despite the the pioneer work by Seilacher (see also links are not possible to establish in the impressive growth of fields exploring other Crimes, 1974). Subsequent ichnologic com- case of ichnofossils having less distinct sources of data (e.g., molecular), the fossil pilations focused on specific environments morphologic features. The trace-fossil record record is arguably still the main line of (e.g., Buatois et al., 1998; Orr, 2001; Uchman, encompasses marine and continental evidence to reconstruct the diversity of life 2004; Minter et al., 2016a, 2016b, 2017) environments and spans from Ediacaran to through time (Valentine, 1969; Raup, 1972, or evolutionary radiations (e.g., Mángano Holocene (Buatois and Mángano, 2016). GSA Today, v. 28, https://doi.org/10.1130/GSATG371A.1. Copyright 2018, The Geological Society of America. CC-BY-NC. Cl Figure 1. Ichnologic equivalents of Sepkoski’s CAMBRIAN EVOLUTIONARY evolutionary faunas. Representative elements FAUNA Li of the Cambrian evolutionary fauna include Ru Sy trilobite trace fossils, such as Rusophycus (Ru), Cruziana (Cr) and Dimorphichnus (Di), and the Cr Di inarticulate brachiopod burrow Lingulichnus (Li). Trace fossils of worm-like organisms Ol include Syringomorpha (Sy) and Oldhamia (Ol), whereas Climactichnites (Cl) has been attributed to mollusk-like producers. Examples of the Paleozoic evolutionary fauna include Da ichnotaxa produced by worm-like animals, such as Daedalus (Da), Arthrophycus (Ar), PALEOZOIC EVOLUTIONARY FAUNA Heimdallia (He), and Dictyodora (Dy). The Ar He Modern evolutionary fauna is dominated by crustacean burrows, such as Psilonichnus (Ps), Ophiomorpha (Op), Thalassinoides (Th), and Dy Sinusichnus (Si), as well as bivalves, such as Hillichnus (Hi), and irregular echinoids, such as Scolicia (Sc). Structures produced by worm-like organisms include Lapispira (La), Schaubcylindrichnus (Sch), Phoebichnus (Ph), Ha Si and Haentzschelinia (Ha). For bibliographic Ps Op sources, see supplementary material in the Sch GSA Data Repository (see text footnote 1). MODERN EVOLUTIONARY FAUNA Ph Th La Sc Sc Hi Whereas the main focus of studies on that taxonomy is more firmly established nonmarine clastic rock volume, the number biodiversity has been on the number of at ichnogenus level than at ichnospecies of ichnofossil-bearing formations, and species or higher taxa (Sepkoski, 1997), rank. Only invertebrate trace-fossil data the number of trace-fossil assemblages ichnodiversity (or trace-fossil diversity) were considered. Individual curves were documented (Minter et al., 2017). Potential studies focus on the different behaviors produced for continental, shallow-marine, biases are discussed in the supplementary involved in animal-substrate interactions. and deep-marine bioturbation, and material (see footnote 1). Ichnodiversity refers to the number of marine and continental bioerosion (Fig. 2). trace-fossil types (ichnotaxa) present in Additional diversity curves were compiled RESULTS any given assemblage or geologic period, for all marine bioturbation, all marine Behavioral innovations seem to have taken therefore providing a measurement of (bio erosion plus bioturbation), and all place in pulses rather than at a steady pace behavioral richness (Bua tois and Mángano, continental (bioerosion plus bioturbation) (Fig. 2). For marine environments, a 433% 2011, 2013). Ichnogeneric compilation was ichnogenera. A rarefaction analysis of increase in ichnodiversity occurred during based on literature and personal data (GSA the data pertaining to the Cambrian and the Terraneuvian, a 48% increase took place Data Repository Tables DR1 and DR21). The Ordovician portions of the marine curves between the Early and Late Ordovician, total number of invertebrate ichnogenera showing rapid ichnodiversity increases was and a more protracted and modest identified as valid is 534, encompassing undertaken to evaluate the effects of increase occurred later in the Mesozoic with 428 for bioturbation structures and 106 for sample size on the curves (Buatois et al., increases in the Early Jurassic (8%) and bioerosion structures (updated from Buatois 2016a). Diversity data for the continental Late Cretaceous (20%), totaling an overall et al., 2017). We follow the common practice Paleozoic