Skip to main content
SpringerLink
Log in

Ecological drivers of the Ediacaran-Cambrian diversification of Metazoa

  • Original Paper
  • Published:
Evolutionary Ecology Aims and scope Submit manuscript

Abstract

Organismal modifications to their physical and chemical environment play a significant role in structuring many modern ecosystems, and experimental evidence suggests that such behavior can increase diversity. Despite the important role such activities play in connecting ecology and evolution, less is known of the macroevolutionary impact of such influences, especially their role during major evolutionary transitions. The Ediacaran-Cambrian diversification of Metazoa encompassed the appearance and early diversification of virtually all major clades of marine animals and the establishment of metazoan-dominated ecosystems. Here we assess the role of positive ecological feedbacks using a new compilation of the first occurrences of all metazoan phyla, classes; orders and equivalent stem taxa, as well as data from a previously published compendium on fossils from the early to middle Cambrian of China. The results reveal relatively minor feedback during the Ediacaran, but a substantial increase during the Cambrian, principally through bioturbation and the appearance of a number of structural engineers, including sponges. Chemical modification of the environment through filtering and bioturbation seems to have had the largest impact. Data on taxic diversity is a poor proxy for abundance, or for the actual environmental impact of these activities, however. Future assessments of the influence of ecological feedbacks on this event will require standardized assessments of the abundance of taxa with different ecological roles.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Altieri AH, van Wesennbeek B, Bertness MD, Sillman BR (2010) Facilitation cascade drives positive relationship between native biodiversity and invasion sucess. Ecology 91:1269–1275

    Article  PubMed  Google Scholar 

  • Babcock LE, Peng SC (2007) Cambrian chronostratigraphy: current state and future plans. Palaeogeog Palaeoclimat Palaeoecol 254:62–66

    Article  Google Scholar 

  • Bengtson S (2005) Mineralized skeletons and early animal evolution. In: Briggs DEG (ed) Evolving form and function: fossils and development. Peabody Museum of Natural History, New Haven, pp 101–124

    Google Scholar 

  • Berke SK (2010) Functional groups of ecosystem engineers: a proposed classification with comments on current issues. Int Comp Biol 50:147–157

    Article  Google Scholar 

  • Bottjer DJ, Hagadorn JW, Dornbos SQ (2000) The Cambrian substrate revolution. GSA Today 10:1–7

    Google Scholar 

  • Breitburg DL, Crump BC, Dabiri JO, Gallegos CL (2010) Ecosystem engineers in the pelagic realm: alteration of habitat by species ranging from microbes to jellyfish. Int Comp Biol 50:188–200

    Article  Google Scholar 

  • Butterfield NJ (1997) Plankton ecology and the proterozoic–phanerozoic transition. Paleobiology 23:247–262

    Google Scholar 

  • Catling DC, Glein CR, Zahnle KJ, McKay CP (2005) Why O2 is required by complex life on habitable planets and the concept of planetary “oxygenation time”. Astrobiology 5:415–437

    Article  PubMed  CAS  Google Scholar 

  • Chen JY (2009) The sudden appearance of diverse animal body plans during the Cambrian explosion. Int J Dev Biol 53:733–751

    Article  PubMed  Google Scholar 

  • Cuddington K, Wilson WG, Hastings A (2009) Ecosystem engineers: feedback and population dynamics. Am Nat 173:488–498

    Article  PubMed  CAS  Google Scholar 

  • Dame RF, Prins TC (1998) Bivalve carrying capacity in coastal ecosystems. Aquat Ecol 31:409–421

    Article  Google Scholar 

  • Dame RF, Bushek D, Prins TC (2001) Benthic suspension feeders as determinants of ecosystem structure and function in shallow coastal waters. In: Reise K (ed) Ecological comparisons of sedimentary shores. Verlag, Berlin, pp 1–37

    Google Scholar 

  • Davidson EH, Erwin DH (2010) Evolutionary innovation and stability in animal gene networks. J Exp Zool (Mol Dev Evol) 312B:1–5

    Google Scholar 

  • Dewar WK, Bingham RJ, Iverson RL, Nowacek DP, Laurent LC, Wiebe PH (2006) Does the marine biosphere mix the ocean? J Mar Res 64:541–551

    Article  Google Scholar 

  • Diaz MC, Rutzler K (2001) Sponges: an essential component of Caribbean coral reefs. Bull Mar Sci 69:535–546

    Google Scholar 

  • Droser ML, Bottjer DJ (1989) Ordovician increase in extent and depth of bioturbation: implications for understanding early Paleozoic ecospace utilization. Geology 17:850–852

    Article  Google Scholar 

  • Erwin DH (1992) A preliminary classification of evolutionary radiations. Hist Biol 6:133–147

    Article  Google Scholar 

  • Erwin DH (2005) The origin of animal body plans. In: Briggs DEG (ed) Evolving form and function: fossils and development. Peabody Museum of Natural History, New Haven, pp 67–80

    Google Scholar 

  • Erwin DH (2007) Increasing returns, ecological feedback, and the early Triassic recovery. Palaeoworld 16:9–15

    Article  Google Scholar 

  • Erwin DH (2008) Macroevolution of ecosystem engineering, niche construction and diversity. Trends Ecol Evol 23:304–310

    Article  PubMed  Google Scholar 

  • Erwin DH (2009) Early origin of the bilaterian developmental toolkit. Philos Trans R Soc Lond B Biol Sci 364:2253–2261

    Article  PubMed  CAS  Google Scholar 

  • Erwin DH (2011) Evolutionary uniformitarianism. Developmental biology, (in press). http://www.dx.doi.org/10.1016/j.ydbio.2011.01.020

  • Erwin DH, Valentine JW (2012) The Cambrian explosion: the construction of animal biodiversity. Roberts and Co, Greenwood

    Google Scholar 

  • Erwin DH, Valentine JW, Sepkoski JJ Jr (1987) A comparative study of diversification events: the early Paleozoic versus the Mesozoic. Evolution 41:1177–1186

    Article  PubMed  CAS  Google Scholar 

  • Erwin DH, Laflamme M, Tweedt SM, Sperling EA, Pisani D, Peterson KJ. The Cambrian conundrum: early divergence and later ecological success in the early history of animals (in review)

  • Fedonkin MA, Simonetta A, Ivantsov AY (2007) New data on kimberella, the vendian mollusc-like organism (White sea region, Russia): paleontological and evolutionary implications. In: Vickers-Rich P, Komarower P (eds) The rise and fall of the ediacaran biota. Geological Society, London, pp 157–179

    Google Scholar 

  • Gehling JG, Droser ML (2009) Textured organic surfaces associated with the ediacara biota in south Australia. Earth Sci Rev 96:196–206

    Article  CAS  Google Scholar 

  • Gill JM, Coma R (1998) Benthic suspension feeders: their paramount role in littoral marine food webs. Trends Ecol Evol 13:316–321

    Article  Google Scholar 

  • Gutierrez JL, Jones CG, Strayer DL, Iribarne OO (2003) Mollusks as ecosystem engineers: the role of shell production in aquatic habitats. Oikos 101:79–90

    Article  Google Scholar 

  • Hagadorn JW, Bottjer DJ (1997) Wrinkle structures: microbially mediated sedimentary structures common in subtidal siliciclastic settings at the proterozoic–phanerozoic transition. Geology 25:1047–1050

    Article  Google Scholar 

  • Halverson GP, Hurtgen MT, Porter SM, Collins AS (2009) Neoproterozoic-Cambrian biogeochemical evolution in Neoproterozoic-Cambrian tectonics, global change and evolution: a focus on southwestern. In: Gondawana Gaucher C, Sial AN, Halverson GP, Frimmel HE (eds) Developments in Precambrian geology. Elsevier, USA, pp 351–365

    Google Scholar 

  • Ivantsov AY (2009) New reconstruction of kimberella, problematic vendian metazoan. Paleontol J 43:601–611

    Article  Google Scholar 

  • Jackson JB (2001) What was natural in the coastal oceans? Proc Natl Acad Sci USA 98:5411–5418

    Article  PubMed  CAS  Google Scholar 

  • Jensen S, Droser ML, Gehling JG (2005) Trace fossil preservation and the early evolution of animals. Palaeogeog Palaeoclimat Palaeoecol 220:19–29

    Article  Google Scholar 

  • Jensen S, Droser ML, Gehling JG (2006) A critical look at the ediacaran trace fossil record. In: Xiao S, Kaufmane AJ (eds) Neoproterozoic geobiology and paleobiology. Springer, Berlin, pp 115–157

    Chapter  Google Scholar 

  • Jones CG, Gutierrez JL (2007) On the meaning, usage and purpose of the ecosystem engineering concept. In: Cuddington K, Byers JE, Wilson WG, Hastings A (eds) Ecosystem engineers: plants–protists. Academic Press, NY, pp 3–24

    Chapter  Google Scholar 

  • Jones CG, Lawton JH, Shachak M (1994) Organisms as ecosystem engineers. Oikos 69:373–386

    Article  Google Scholar 

  • Jones CG, Lawton JH, Shachak M (1997) Positive and negative effects of organisms as physical ecosystem engineers. Ecology 78:1946–1957

    Article  Google Scholar 

  • Katija K, Dabiri JO (2009) A viscosity-enhanced mechanism for biogenic ocean mixing. Nature 460:624–626

    Article  PubMed  CAS  Google Scholar 

  • Kiessling W (2008) Sampling-standardized expansion and collapse of reef building in the phanerozoic. Foss Rec 11:7–18

    Article  Google Scholar 

  • Knoll AH, Carroll SB (1999) Early animal evolution: emerging views from comparative biology and geology. Science 284:2129–2137

    Article  PubMed  CAS  Google Scholar 

  • Krakauer DC, Page KM, Erwin DH (2009) Diversity, dilemmas and monopolies of niche construction. Am Nat 173:26–40

    Article  PubMed  Google Scholar 

  • Laflamme M, Xiao S, Kowalewski M (2009) Osmotrophy in modular ediacara organisms. Proc Natl Acad Sci USA 106:14438–14443

    Article  PubMed  CAS  Google Scholar 

  • Laland KN, Sterelny K (2006) Seven reasons (not) to neglect niche construction. Evolution 60:1751–1762

    PubMed  Google Scholar 

  • Laland KN, Odling-Smee FJ, Feldman MW (1999) Evolutionary consequences of niche construction and their implications for ecology. Proc Natl Acad Sci USA 96:10242–10247

    Article  PubMed  CAS  Google Scholar 

  • Li GX, Steiner M, Zhu XJ, Yang A, Wang HF, Erdtmann BD (2007) Early Cambrian metazoan fossil record of south China: generic diversity and radiation patterns. Palaeogeog Palaeoclimat Palaeoecol 254:229–249

    Article  Google Scholar 

  • Lohrer AM, Thrush SF, Gibbs MM (2004) Bioturbators enhance ecosystem function through complex biogeochemical interactions. Nature 431:1092–1095

    Article  PubMed  CAS  Google Scholar 

  • Losos JB (2010) Adaptive radiation, ecological opportunity, and evolutionary determinism. Am Nat 175:623–639

    Article  PubMed  Google Scholar 

  • Love GD, Grosjean E, Stalvies C, Fike DA, Grotzinger JP, Bradley AS, Kelly AE, Bhatia M, Meredith W, Snape CE, Bowring SA, Condon DJ, Summons RE (2009) Fossil steroids record the appearance of demospongiae during the cryogenian period. Nature 457:718–721

    Article  PubMed  CAS  Google Scholar 

  • Maloof AC, Porter SM, Moore JL, Dudas FO, Bowring SA, Higgins JA, Fike DA, Eddy MP (2010a) The earliest Cambrian record of animals and ocean geochemical change. GSA Bull 122:1731–1774

    Article  CAS  Google Scholar 

  • Maloof AC, Rose CV, Beach R, Samuels BM, Calmet CC, Erwin DH, Poirier GR, Yao N, Simons FJ (2010b) Possible animal-body fossils in pre-marinoan limestones from south Australia. Nat Geosci 3:653–659

    Article  CAS  Google Scholar 

  • Mangano MG, Buatois LA (2007) Trace fossils in evolutionary paleoecology. In: Miller WF III (ed) Trace fossils: concepts, problems, prospects. Elsevier, Amsterdam, pp 391–411

    Google Scholar 

  • Marshall CR (2006) Explaining the Cambrian “explosion” of animals. Ann Rev Ecol Evol Syst 34:355–384

    CAS  Google Scholar 

  • Mermillod-Blondin F, Rosenberg R (2006) Ecosystem engineering: the impact of bioturbation on biogeochemical processes in marine and freshwater benthic habitats. Aquatic Sci 68:434–442

    Article  CAS  Google Scholar 

  • Narbonne GM (2005) The ediacara biota: neoproterozoic origin of animals and their ecosystems. Ann Rev Earth Planet Sci 33:421–442

    Article  CAS  Google Scholar 

  • Newell RIE (1988) Ecological changes in Chesapeake Bay: are they the result of overharvesting the American oyster, C. virginica?. Chesapeake Bay Consortium, Baltimore

    Google Scholar 

  • Newell RIE (2004) Ecosystem influences of natural and cultivated populations of suspension-feeding bivalve molluscs: a review. J Shellfish Res 23:51–61

    Google Scholar 

  • Nogaro G, Mermillod-Blondin F, Valett MH, Francois-Carcaillet F, Gaudet JP, Lafont M, Gibert J (2009) Ecosystem engineering at the sediment–water interface: bioturbation and consumer-substrate interaction. Oecologia 161(1):125–138

    Article  PubMed  Google Scholar 

  • Odling-Smee FJ, Laland KN, Feldman MW (2003) Niche construction: the neglected process in evolution. Princeton University Press, Princeton

    Google Scholar 

  • Ostroumov SA (2005) Some aspects of the water filtering activity of filter feeders. Hydrobiologia 542:275–286

    Article  CAS  Google Scholar 

  • Post DM, Palkovacs EP (2009) Eco-evolutionary feedbacks in community and ecosystem ecology: interactions between the ecological theater and the evolutionary play. Phil Trans R Soc Lond B 364:1629–1640

    Article  Google Scholar 

  • Reiswig HM (1971) Particle feeding in natural populations of three marine demon sponges. Biol Bull 141:568–591

    Article  Google Scholar 

  • Schields-Zhou G, Och L (2011) The case for a neoproterozoic oxygenation event: geochemical evidence and biological consequences. GSA Today 21:4–11

    Article  Google Scholar 

  • Schluter D (2000) The ecology of adaptive radiation. Oxford University Press, Oxford

    Google Scholar 

  • Seilacher A, Pfluger F (1994) From biomats to benthic agriculture: a biohistoric revolution. In: Krumbein W, Paterson DM, Stal LJ (eds) Biostablization of sediments. Bibliotheks-und Informationssystem der Universität Oldenburg, Oldenbueg, pp 97–105

    Google Scholar 

  • Seilacher A, Buatois LA, Mangano MG (2005) Trace fossils in the Ediacaran-Cambrian transition: behavioral diversification, ecological turnover and environmental shift. Palaeogeog Palaeoclimat Palaeoecol 227:323–356

    Article  Google Scholar 

  • Sepkoski JJ Jr (1992) A compendium of fossil marine animal families, 2nd edn. Milwaukee Pub Mus Contrib Biol Geol 83:155

    Google Scholar 

  • Sepkoski JJ Jr (2002) A compendium of fossil marine animal genera. Bull Am Paleo 363:1–560

    Google Scholar 

  • Sepkoski Jr JJ (1995) The ordovician radiations: diversification and extinction shown by global genus-level taxonomic data. Ordovician symposium

  • Servais T, Owen AW, Harper DAT, Kroger B, Munnecke A (2010) The great ordovician biodiversification event (GOBE): the palaeoecological dimension. Palaeogeog Palaeoclimat Palaeoecol 294:99–119

    Article  Google Scholar 

  • Simpson GG (1953) The major features of evolution. Columbia University Press, NY

    Google Scholar 

  • Sperling EA, Vinther J (2010) A placazoan affinity for dickinsonia and the evolution of late Proterozoic metazoan feeding modes. Evol Dev 12:201–209

    Article  PubMed  Google Scholar 

  • Sperling EA, Pisani D, Peterson KJ (2007) Poriferan paraphyly and its implications for Precambrian palaeobiology. In: Vickers-Richard P, Komarower P (eds) The rise and fall of the ediacaran biota. Geological Society, London, pp 355–368

    Google Scholar 

  • Sperling EA, Peterson KJ, Laflamme M (2011) Rangeomorphs, thectardis (porifera?) and dissolved organic carbon in the ediacaran oceans. Geobiology 9:24–33

    Article  PubMed  CAS  Google Scholar 

  • Ulanowicz RE, Tuttle JH (1992) The trophic consequences of oyster stock rehabilitation in Chesapeake Bay. Estuaries 15:298–306

    Article  CAS  Google Scholar 

  • Vogel S (1977) Current-induced flow through living sponges in nature. Proc Nat Acad Sci USA 74:2069–2071

    Article  PubMed  CAS  Google Scholar 

  • Webby BD (2004) Introduction. In: Webby BD, Paris F, Droser MD, Percival IG (eds) The great ordovician biodiversification event. Columbia University Press, NY, pp 1–37

    Google Scholar 

  • Webby BD, Paris F, Droser MD, Percival IG (eds) (2004) The great Ordovician biodiversification event. Columbia University Press, NY

    Google Scholar 

  • Wright JP, Jones CG (2006) The concept of organisms as ecosystem engineers 10 years on: progress, limitations, and challenges. Bioscience 56:203–209

    Article  Google Scholar 

  • Xiao SH, Laflamme M (2008) On the eve of animal radiation: phylogeny, ecology and evolution of the ediacara biota. Trends Ecol Evol 24:31–40

    Article  PubMed  Google Scholar 

  • Yoder JB, Clancey E, Des Roches S, Eastman JM, Gentry L, Godsoe W, Hagey TJ, Oswald BP, Robertson J, Sarver BAJ, Schenks JJ, Spear SF, Harmon LJ (2010) Ecological opportunity and the origin of adaptive radiation. J Evol Biol 23:1581–1596

    Article  PubMed  CAS  Google Scholar 

  • Zhu MY, Babcock LE, Peng SC (2009) Advances in Cambrian stratigraphy and paleontology: integrating correlation techniques, paleobiology, taphonomy and paleoenvironmental reconstruction. Paleoworld 15:217–222

    Article  Google Scholar 

Download references

Acknowledgments

This paper is dedicated to Jeremy Jackson, in thanks for many long arguments over the years about evolutionary ecology. We acknowledge support from the NASA National Astrobiology Institute, discussions with D. Krakauer and J. Odling-Smee, the suggestions of P. Wagner and M. Kosnik, and comments from S. Burke and an anonymous reviewer.

Author information

Authors and Affiliations

  1. Department of Paleobiology, MRC-121, National Museum of Natural History, P.O. Box 37012, Washington, DC, 20013-7012, USA

    Douglas H. Erwin & Sarah Tweedt

  2. Santa Fe Institute, 1399 Hyde Park Road, Santa Fe, NM, 87501, USA

    Douglas H. Erwin

  3. Behavior, Ecology, Evolution and Systematics (BEES), University of Maryland, College Park, MD, 20742, USA

    Sarah Tweedt

Authors
  1. Douglas H. Erwin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sarah Tweedt
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Douglas H. Erwin.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Erwin, D.H., Tweedt, S. Ecological drivers of the Ediacaran-Cambrian diversification of Metazoa. Evol Ecol 26, 417–433 (2012). https://doi.org/10.1007/s10682-011-9505-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10682-011-9505-7

Keywords

Search

Navigation