INNVITEDVITED REEVIEWVIEW ARRTICLETICLE The earliest Cambrian record of animals and ocean geochemical change Adam C. Maloof1,†, Susannah M. Porter2, John L. Moore2, Frank Ö. Dudás3, Samuel A. Bowring3, John A. Higgins1, David A. Fike4, and Michael P. Eddy1 1Department of Geosciences, Princeton University, Guyot Hall, Washington Road, Princeton, New Jersey 08544, USA 2Department of Earth Science, University of California, Santa Barbara, California 93106, USA 3Department of Earth, Atmospheric and Planetary Sciences, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139, USA 4Department of Earth and Planetary Sciences, Washington University, St. Louis, Missouri 63130, USA ABSTRACT are associated with rapid reorganizations of of macroscopic Ediacara fossils (e.g., Tyler the carbon cycle, and are superimposed on and Barghoorn, 1954; Barghoorn and Tyler, The Cambrian diversifi cation of animals long-term increases in sea level and the hydro- 1965; Ford, 1958; Glaessner and Wade, 1966; was long thought to have begun with an explo- thermal fl ux of Sr. Schopf, 2000) helped solve this conundrum, sive phase at the start of the Tommotian Age. but the sudden diversity of the Cambrian fos- Recent stratigraphic discoveries, however, INTRODUCTION sil record remained a puzzle (cf. Cloud, 1948, suggest that many taxa appeared in the older 1965). Despite abundant evidence for a vari- Nemakit-Daldynian Age, and that the diver- In his book On the Origin of Species, Charles ety of life extending back to at least 3.5 Ga, sifi cation was more gradual. We map lowest Darwin suggested that one of the greatest chal- Precambrian fossils mostly record the evo- Cambrian (Nemakit-Daldynian through Tom- lenges to his ideas was the “sudden appearance lution of bacteria and microbial eukaryotes . δ13 motian) records of CCaCO3 variability from of groups of Allied Species in the lowest known The earliest evidence for animals predates Siberia, Mongolia, and China onto a Moroc- fossiliferous strata” (Darwin, 1859, p. 306). He the Precambrian-Cambrian boundary by δ13 can U/Pb– CCaCO3 age model constrained wrote (Darwin, 1859, p. 307): only ~100 m.y. (Xiao et al., 1998; Yin et al., by fi ve U/Pb ages from inter bedded volcanic 2007; Love et al., 2009, Maloof et al., 2010b), ashes. The δ13C correlations ignore fos- “… if my theory be true, it is indisputable that before and the few unquestioned examples of Pre- CaCO3 the lowest Silurian stratum was deposited, long peri- sil tie points, so we assume synchro neity in ods elapsed, as long as, or probably far longer than, cambrian Bilateria are <15 m.y. older than δ13C trends rather than synchroneity in fi rst the whole interval from the Silurian age to the pres- the beginning of the Cambrian (Fedonkin and appearances of animal taxa. We pre sent new ent day; and that during these vast, yet quite unknown, Waggoner , 1997; Martin et al., 2000; Jensen , δ13C , 87Sr/86Sr, uranium, and vanadium data periods of time, the world swarmed with living crea- 2003; Droser et al., 2005). Signifi cant increases org tures. … To the question why we do not fi nd records from the same carbonate samples that defi ne of these vast primordial periods, I can give no satisfac- in trace fossil diversity and complexity across δ13 the Moroccan CCaCO3 curve. The result is tory answer.” the boundary and the absence of soft-bodied a new absolute time line for fi rst appear- ani mals in upper Precambrian Burgess Shale– ances of skeletal animals and for changes in The dilemma Darwin faced was that if all type biotas (Xiao et al., 2002) suggest that the the carbon, strontium, and redox chemistry life descended via gradual modifi cation from general absence of bilaterian animal fossils from of the ocean during the Nemakit-Daldynian a single common ancestor, then the complex- upper Precambrian rocks is not a preservational and Tommotian ages at the beginning of ity and diversity of fossils found in Cambrian artifact. Rather, it appears that animals origi- the Cambrian. The time line suggests that strata (at that time referred to the lower part nated and began to diversify relatively close to the diversifi cation of skeletal animals began of the Silurian) demand a long interval of evo- the base of the Cambrian. Although early stud- early in the Nemakit-Daldynian, with much lution prior to the beginning of the Cambrian. ies using a “molecular clock” suggested that of the diversity appearing by the middle of During Darwin’s time, there was no evidence the divergences between major animal groups the age. Fossil fi rst appearances occurred in of this life, and all that he could offer as expla- long predated the Cambrian (Wray et al., 1996; three pulses, with a small pulse in the earliest nation was the incompleteness of the geologi- Bromham et al., 1998), some of the more recent Nemakit-Daldynian (ca. 540–538 Ma), a larger cal record: The interval of time during which work has produced dates that are closer to (if pulse in the mid- to late Nemakit-Daldynian the ancestors to trilobites, brachiopods, mol- still older than) those supported by the fossil (ca. 534–530 Ma), and a moderate pulse in the luscs, and other Lower Cambrian taxa evolved record (Aris-Brosou and Yang, 2003; Peterson Tommotian (ca. 524–522 Ma). These pulses is not preserved in the rock record. et al., 2004, 2008). Further more, Konservat- Beginning in the 1950s, discoveries of Pre- Lagerstätten such as the Cheng jiang biota and †E-mail: [email protected] cambrian microfossils in chert and shale and the Burgess Shale record a breathtaking array GSA Bulletin; November/December 2010; v. 122; no. 11/12; p. 1731–1774; doi: 10.1130/B30346.1; 20 fi gures; 4 tables; Data Repository item 2010293. For permission to copy, contact [email protected] 1731 © 2010 Geological Society of America Downloaded from https://pubs.geoscienceworld.org/gsa/gsabulletin/article-pdf/122/11-12/1731/3400785/1731.pdf by Princeton University user on 09 September 2019 Maloof et al. of soft-bodied animals by the late Early and Lower Cambrian fossils indicate that diver- et al., 1996). Although of signifi cant interest, Middle Cambrian (Briggs et al., 1994; Hou gences among the major groups of animals this high disparity soon after a group’s appear- et al., 2004), respectively, and, together with must have occurred by that time, the assembly ance is not unique to the Cambrian. more conventional skeletal assemblages, sug- of the major animal body plans—the suites The second puzzling aspect of the Cambrian gest a great radiation of animal life during the of characters that defi ne the living phyla—in explosion, the high rate of diversifi cation, ap- Early Cambrian. many cases took longer (Budd and Jensen, pears to be in part an artifact of a frequently These observations led scientists to focus in 2000). In other words, crown-group represen- incomplete Cambrian record with a dearth of re- particular on two puzzling aspects of the Cam- tatives of most phyla (i.e., those that possess liable radiometric age constraints. Using radio- brian radiation, both encompassed by the term all of the characters of the living groups) fi rst metric dates of volcanic ash units inter bedded in “Cambrian explosion” (cf. Marshall, 2006). appear later than the Early Cambrian, and in fossiliferous strata, workers discovered that the The fi rst is the dramatic increase in disparity some cases much later. Most Early Cambrian base of the Cambrian is ca. 542 Ma (Bowring (morphological distinctness) as represented by animals are, in fact, the intermediate taxa or et al., 1993; Grotzinger et al., 1995; Bowring the supposed appearance of nearly all major stem-groups that were thought to be miss- et al., 2007), rather than 570 Ma (Harland et al., animal body plans (equivalent to the animal ing from the early animal record (Budd and 1990) or ca. 600 Ma (Holmes, 1960; Harland phyla) within a geologically brief interval of Jensen , 2000; Conway Morris and Peel, 1995; et al., 1982). This newly compressed Cam- time near the beginning of the Cambrian (e.g., Shu et al., 2001; Budd, 2002; Caron et al., brian Period led numerous authors to conclude Gould, 1989; Valentine, 1994, 2002, 2004). 2006; Skovsted et al., 2008). that diversifi cation rates had to be twice as fast This problem was compounded by an apparent Nonetheless, it is true that many Early Cam- as they already were thought to be. Despite lack of evidence for “intermediate” taxa—taxa brian taxa are at least recognizably related to these new geochronological constraints on the that lie close to the last common ancestor of crown-group phyla, suggesting that many of the Ediacaran-Cambrian (E-C) boundary and the different phyla in the metazoan tree (Marshall, basic features that distinguish the major groups length of the Cambrian Period, the duration 2006). The second diffi culty is the high rate of of animals had evolved by this time (Budd, of individual Cambrian stages associated with diversifi cation (increase in number of species) 2008). In other words, the Early Cambrian diver- specifi c animal radiations remained poorly con- in the Early Cambrian, particularly the appar- sifi cation of animals is marked by high disparity. strained. Additional U/Pb dating of zircons in ent spike in diversifi cation during the Tommo- However, the observation that disparity reaches volcanic ash layers demonstrated that the Early tian and Atdabanian ages (Fig. 1), spanning an its peak early in a group’s history seems to re- Cambrian is in fact quite long, spanning 32 m.y. interval that seemed short relative to subsequent fl ect a general phenomenon, also observed in and nearly 60% of Cambrian time (Bowring radiations (e.g., Sepkoski, 1992; Zhuravlev, plants (Boyce, 2005), the Ediacara biota (Shen et al., 1993; Grotzinger et al., 1995; Landing 2001; Marshall, 2006).