Journal of Earth Science, Vol. 21, Special Issue, p. 21–24, June 2010 Printed in China
ISSN 1674-487X
The Cambrian Substrate Revolution and Early Evolution of the Phyla David J Bottjer* Department of Earth Sciences, University of Southern California, Los Angeles, CA 90089-0740, USA ABSTRACT: Evidence from Precambrian carbonate and siliciclastic sedimentary structures indicates that in marine settings before the Cambrian conditions of seafloor environments were largely controlled by microbes and the mats which they form. During the Ediacaran–Cambrian transition, a vertical component to marine bioturbation evolved, as well as overall increased seafloor bioturbation. The “Cambrian substrate revolution (CSR)” encompasses the evolutionary and ecological effects that occurred due to these substrate changes. The continued evolution of bioturbating organisms caused the development of a significant variety of new microenvironments, which led to the formation of new ecospace and evolutionary opportunities for other benthic organisms. Numerous studies have evaluated the “weird” morphology of early seafloor animals and how they adapted to an increasingly bioturbated substrate. Many early animals adapted to seafloors with strong microbial mat development are stem groups of the phyla we recognize today, and thus have morphological features absent in modern representatives. Fossils of crown groups of modern phyla first began to appear in the Cambrian and subsequently dominated Phanerozoic bioturbated seafloor environments. The CSR is thus a primary component of the evolution of stem and crown groups of the phyla during the Cambrian explosion. KEY WORDS: Cambrian substrate revolution, Cambrian explosion, stem group, crown group, bioturbation, Ediacaran.
INTRODUCTION The Cambrian explosion is noted as the first appearance in the fossil record of many of the phyla which characterize today’s oceans (e.g., Valentine, 2004). But, when applying a cladistic methodology, most of these Cambrian organisms are stem groups in the total group that comprises each of these phyla. It is also likely that animals in the earlier Ediacara biota represent stem groups of the modern phyla (e.g., Peterson et al., 2008; Xiao and Laflamme, 2008). *Corresponding author:
[email protected] © China University of Geosciences and Springer-Verlag Berlin Heidelberg 2010 Manuscript received December 20, 2009. Manuscript accepted February 20, 2010.
Changing ecology played a strong role in the development of the Cambrian explosion (e.g., Marshall, 2006; Bottjer et al., 2000). An important question in understanding the early evolution of animals is what role changing ecology played in the evolution of stem and crown groups of phyla from the Ediacaran through the Early Paleozoic. CAMBRIAN SUBSTRATE REVOLUTION Microbially-mediated sedimentary structures and microbialites are common in rocks of the Ediacaran and Early Cambrian and are comparatively scarce in younger rocks (e.g., Gehling, 1999; Hagadorn and Bottjer, 1999, 1997). This implies that most seafloor sediments in the Ediacaran through Early Cambrian were bound together by microbial filaments, making them firmer and more cohesive than those of the
22
modern oceans (e.g., Gehling, 1999; Hagadorn and Bottjer, 1997). These “matgrounds” would likely have been difficult or impossible for benthic metazoans to penetrate, and the combination of ubiquitous mats and a lack of infaunal bioturbation would have prevented aeration of the sediment, allowing an oxic-anoxic boundary to develop in the sediment close to the seafloor surface (McIlroy and Logan, 1999). As a result, all metazoan activities likely took place on the top surfaces of mats, within mats, or immediately beneath them. Seilacher (1999) proposed four guilds to characterize the categories of metazoan activity that took place in Ediacaran shallow marine benthic communities. These are mat encrusters, organisms that lived permanently attached to the mat surface; mat scratchers, mobile organisms that scavenged or hunted for food on the surface of the mat without damaging it; mat stickers, suspension feeders that used conical shells to maintain an upright orientation in the surface of the mat; and undermat miners, burrowers that tunneled directly beneath the mat and fed on detritus from the layers above (Seilacher, 1999). A transition occurred during the Cambrian between seafloors that were characterized by primarily horizontal bioturbation and extensive microbial mats and those that were characterized by extensive vertical bioturbation and absent microbial mats. Seilacher and Pflüger (1994) proposed the “agronomic revolution” hypothesis to explain how and why this transition in seafloor conditions and benthic behavior took place. According to this hypothesis, benthic metazoans acquired evolutionary adaptations during the Cambrian explosion that allowed them to burrow vertically into matgrounds. Bioturbation depth and intensity increased, eventually disrupting the layered structure of the microbial mats and increasing the water and oxygen content of the seafloor sediment. Mat development was relegated to marginal environments in the wake of the agronomic revolution, and the seafloor took on characteristics more typical of post-Cambrian marine settings, such as improved nutrient distribution and an indistinct water-sediment boundary (Bottjer et al., 2000). The ecological and evolutionary effects of the agronomic revolution are reflected in the record of
David J Bottjer
body and trace fossils and have been termed collectively the “Cambrian substrate revolution (CSR)” (Bottjer et al., 2000). With increasing depth and intensity of bioturbation, benthic metazoans brought about a dramatic change in shallow subtidal seafloors of the Early Cambrian, supplanting microbes as the dominant biotic influence on many seafloor conditions and making available to other members of the community a variety of previously inaccessible resources and ecological niches (e.g., Bottjer et al., 2000). EARLY EVOLUTION OF THE PHYLA The oldest evidence for animals from the stratigraphic record comes from biomarkers of sponges that date to ~635 Ma ago (Love et al., 2009). The Doushantuo Formation of Southwest China, dated at 580–600 Ma ago, contains a variety of microfossils variously interpreted as evidence for the presence of sponges, cnidarians, and bilaterians (e.g., Chen et al., 2009). The Ediacara biota, dating from 575 Ma ago until the Precambrian–Cambrian boundary at 542 Ma ago, contains the oldest macrofossils, including several interpreted as bilaterians (e.g., Peterson et al., 2008; Xiao and Laflamme, 2008). The specific biological affinities of all of this evidence for Ediacaran animals are controversial, but it is very likely that they all represent animals that are members of stem groups of the modern phyla (e.g., Peterson et al., 2008). Eleven phyla first appeared in the fossil record in the Cambrian (Valentine, 2004), and this together with the appearance in the Cambrian of diverse body fossils with mineralized skeletons has led to the term “Cambrian explosion”. Many of these Cambrian fossils have unusual morphologies that led to them being perceived as “weird wonders”, that possessed unique body plans restricted to the Cambrian (Brysse, 2008). Application of cladistic analyses, however, has revealed that rather than unique many of these organisms are stem group members of the modern phyla (e.g., Brysse, 2008). A stem group of a phylum includes extinct representatives that do not have all of the characters that are found in modern representatives of that phylum, which constitute the other component of a phylum, the crown groups. Only a few crown group representatives of the phyla occur in the Cambrian (e.g., Zhang et al., 2007).
The Cambrian Substrate Revolution and Early Evolution of the Phyla
Because echinoderms have an excellent fossil record due to their well-mineralized skeletons made of stereom (e.g., Bottjer et al., 2006), they provide a good example of the CSR and early evolution in a phylum. Stem group echinoderms in the Cambrian include eocrinoids, edrioasteroids, and helicoplacoids (Bottjer et al., 2006). Early helicoplacoids, edrioasteroids, and eocrinoids had a sediment sticker mode of life adapted to living on substrates with a low level of bioturbation (e.g., Dornbos, 2006; Bottjer et al., 2000). Later edrioasteroids and eocrinoids adapted to increasing bioturbation by evolving adaptations for attaching to hard substrates (Bottjer et al., 2006; Dornbos, 2006). Helicoplacoids did not evolve adaptations for living on other than soft substrates, and so became extinct later in the Cambrian, coincident with increasing levels of bioturbation (Dornbos and Bottjer, 2000). Crown group members of the echinoderms, crinoids, asteroids, ophiuroids, holothurians, and echinoids, first appear in the Ordovician (e.g., Bottjer et al., 2006) and have mobile or attached life habits that are more suitable to a benthic regime with significant bioturbation (Dornbos, 2006).
23
that are adaptations to the increasingly bioturbated seafloor, and thus it is likely that the changing conditions of increasing bioturbation led to evolution of many of the morphological characters that characterize crown groups of the phyla. ACKNOWLEDGMENTS Thanks to the numerous colleagues who have contributed to development of this research, including Stephen Dornbos, James W. Hagadorn, Katherine Marenco, Eric Davidson, Kevin Peterson, J. William Schopf, Jun-Yuan Chen, Mary Droser, Kirk Domke, and Scott Mata. REFERENCES CITED Bottjer, D. J., Davidson, E. H., Peterson, K. J., et al., 2006. Paleogenomics of Echinoderms. Science, 314: 956–960 Bottjer, D. J., Hagadorn, J. W., Dornbos, S. Q., 2000. The Cambrian Substrate Revolution. GSA Today, 10: 1–7 Brysse, K., 2008. From Weird Wonders to Stem Lineages: The Second Reclassification of the Burgess Shale Fauna. Stud. Hist. Phil. Biol. & Biomed. Sci., 39: 298–313 Chen, J. Y., Bottjer, D. J., Li, G., et al., 2009. Complex Embryos Displaying Bilaterian Characters from Precambrian
CONCLUSIONS Seafloors in the Ediacaran were covered by microbial mats that controlled the physical and chemical nature of the water-sediment interface. Verticallydirected and more extensive bioturbation of the seafloor evolved in the Cambrian, and for much of the Cambrian the seafloor was a mosaic of environments still controlled by the properties of microbial mats, as well as more bioturbated seafloors. Benthic animals in the Ediacaran and Early Cambrian had a suite of adaptations including morphological characters that allowed them to function efficiently on these matbound seafloor environments. Many of these morphological characters can be shown to be those that characterize these organisms as stem group members of the phyla. Bioturbation became deeper and more extensive into the Ordovician and subsequently the remainder of the Phanerozoic. Coincident with this was the first appearance of animals with morphological characters demonstrating that they are ancestors of living animals, and thus crown group representatives of the phyla. Many of these animals have morphological features
Doushantuo Phosphate Deposits, Weng’an, Guizhou, China. Proceedings of the National Academy of Sciences, 106: 19056–19060 Dornbos, S. Q., 2006. Evolutionary Paleoecology of Early Epifaunal Echinoderms: Response to Increasing Bioturbation Levels during the Cambrian Radiation. Palaeogeography, Palaeoclimatology, Palaeoecology, 237: 225–239 Dornbos, S. Q., Bottjer, D. J., 2000. Evolutionary Paleoecology of the Earliest Echinoderms: Helicoplacoids and the Cambrian Substrate Revolution. Geology, 28: 839–842 Gehling, J. G., 1999. Microbial Mats in Terminal Proterozoic Siliciclastics: Ediacaran Death Masks. Palaios, 14: 40–57 Hagadorn, J. W., Bottjer, D. J., 1997. Wrinkle Structures: Microbially Mediated Sedimentary Structures Common in Subtidal
Siliciclastic
Settings
at
the
Proterozoic–
Phanerozoic Transition. Geology, 25: 1047–1050 Hagadorn, J. W., Bottjer, D. J., 1999. Restriction of a Late Neoproterozoic Biotope: Suspect-Microbial Structures and Trace Fossils at the Vendian–Cambrian Transition. Palaios, 14: 73–85 Love, G. D., Grosjean, E., Stalvies, C., et al., 2009. Fossil Steroids Record the Appearance of Demospongiae during the
David J Bottjer
24 Cryogenian Period. Nature, 457: 718–721
Seilacher, A., Pflüger, F., 1994. From Biomats to Benthic Ag-
Marshall, C. R., 2006. Explaining the Cambrian “Explosion” of
riculture: A Biohistoric Revolution. In: Krumbein, W. E.,
Animals. Annual Reviews of Earth and Planetary Science,
Paterson, D. M., Stal, L. J., eds., Biostabilization of Sedi-
34: 355–384
ments. Bibliotheks Und Infomationssystem Der Carl Von
McIlroy, D., Logan, G. A., 1999. The Impact of Bioturbation on
Infaunal
Ecology
and
Evolution
during
the
Proterozoic–Cambrian Transition. Palaios, 14: 58–72
Ossietzky Universität, Oldenburg, Germany. 97–105 Valentine, J. W., 2004. On the Origin of Phyla. University of Chicago Press, 614
Peterson, K. J., Cotton, J. A., Gehling, J. G., et al., 2008. The
Xiao, S., Laflamme, M., 2008. On the Eve of Animal Radiation:
Ediacaran Emergence of Bilaterians: Congruence between
Phylogeny, Ecology and Evolution of the Ediacara Biota.
the Genetic and the Geological Fossil Records. Philoso-
Trends in Ecology and Evolution, 24: 31–40
phical Transactions of the Royal Society B, 363: 1435–1443 Seilacher, A., 1999. Biomat-Related Lifestyles in the Precambrian. Palaios, 14: 86–93
Zhang, X. G., Siveter, D. J., Waloszek, D., et al., 2007. An Epipodite-Bearing Crown-Group Crustacean from the Lower Cambrian. Nature, 449: 595–598