View source for Cambrian substrate revolution

{{redirect-distinguish|Agronomic revolution|Green Revolution (disambiguation){{!}}Green revolution|Agricultural revolution (disambiguation){{!}}Agricultural revolution|Agrarian revolution (disambiguation){{!}}Agrarian revolution}}
{{short description|Diversification of animal burrowing}}
{{Cambrian substrate revolution | caption=Before and after the Cambrian substrate revolution }}{{CEXNAV}}
The "'''Cambrian substrate revolution'''"<ref name="BottjerEtAl2000CambrianSubstrateRevolution">{{cite magazine |author1=Bottjer, D.J. |author2=Hagadorn, J.W. |author3=Dornbos, S.Q. |title=The Cambrian substrate revolution |magazine=GSA Today |volume=10 |issue=9 |date=September 2000 | url=https://www.geosociety.org/gsatoday/archive/10/9/pdf/i1052-5173-10-9-1.pdf | access-date=2008-06-28 | pages=1–9}}</ref> or "'''Agronomic revolution'''",<ref name=Seilacher1994>{{cite book |last1=Seilacher |first1=A. |last2=Pflüger |first2=F. |year=1994 |chapter=From biomats to benthic agriculture: A biohistoric revolution |editor-last=Krumbein |editor-first=W. E. |editor2-last=Peterson |editor2-first=D. M. |editor3-last=Stal |editor3-first=L. J. |title=Biostabilization of Sediments |publisher=Bibliotheks-und Informationssystem der Carl von Ossietzky Universität Oldenburg |pages=97–105 |isbn=3-8142-0483-2 }}</ref> evidenced in [[trace fossil]]s, is a sudden diversification of [[Burrow|animal burrowing]] during the early [[Cambrian]] period.

Before this "widening of the behavioural repertoire",<ref>S. Conway Morris, 2001</ref> [[Benthos|bottom-dwelling]] animals mainly grazed on the [[microbial mat]]s that lined the surface of the substrate, crawling above (like how [[freshwater snail]]s still do) or burrowing just below them. These microbial mats created a barrier between the water and the [[Substrate (marine biology)|sediment underneath]], which was less water-logged than modern sea-floors, and almost completely [[Hypoxia (environmental)|anoxic]] (lacking in [[oxygen]]). As a result, the substrate was inhabited by [[sulfate-reducing bacteria]], whose emissions of [[hydrogen sulfide]] (H<sub>2</sub>S) made the substrate toxic to most other organisms.<ref name="BaileyEtAl2006MicrobiallyMediatedEnvironmentalInfluences">{{cite journal | title=Microbially-Mediated Environmental Influences on Metazoan Colonization of Matground Ecosystems: Evidence from the Lower Cambrian Harkless Formation |author1=Bailey, J.V. |author2=Corsetti, F.A. |author3=Bottjer, D.J. |author4= Marenco, K.N. | journal= PALAIOS| volume=21 |issue=3 |date=June 2006 | doi=10.2110/palo.2005-p05-51e | pages=215 |bibcode=2006Palai..21..215B |s2cid=130690224 }}</ref>

Around the start of the Cambrian, organisms began to burrow vertically, forming a great diversity of different [[fossil]]isable burrow forms and traces as they penetrated the sediment for protection or to feed.<ref name=Seilacher2005>{{cite journal
 | author = Seilacher, Adolf
 |author2=Luis A. Buatoisb |author3=M. Gabriela Mángano
  | date = 2005-10-07
 | title = Trace fossils in the Ediacaran–Cambrian transition: Behavioral diversification, ecological turnover and environmental shift 
 | journal =  	Palaeogeography, Palaeoclimatology, Palaeoecology
 | volume = 227
 | issue = 4
 | pages = 323–356
 | doi = 10.1016/j.palaeo.2005.06.003  
 |bibcode=2005PPP...227..323S }}</ref>
These burrowing animals broke down and weakened the microbial mats, thus allowing water and oxygen to penetrate a considerable distance below the surface. This restricted the sulfate-reducing bacteria and their H<sub>2</sub>S emissions to the deeper layers, making the upper layers of the sea-floor habitable for a much wider range of organisms. The upper level of the sea-floor became wetter and softer as it was constantly churned up by burrowers.<ref name="BottjerEtAl2000CambrianSubstrateRevolution" />

==Burrowing before the Cambrian==

[[File:Ediacaran trace fossil.jpg|thumb|An Ediacaran trace fossil, made when an organism burrowed below a microbial mat]]
The traces of organisms moving on and directly underneath the microbial mats that covered the Ediacaran sea floor are preserved from the [[Ediacaran period]], about {{Ma|565}}.  The only Ediacaran burrows are horizontal, on or just below the surface, and were made by animals which fed above the surface, but burrowed to hide from predators.<ref name=Dzik2007/> If these burrows are [[biogenic]] (made by organisms) they imply the presence of motile organisms with heads, which would probably have been [[bilateria|bilaterians]] (bilaterally symmetrical animals).<ref>{{Cite book
 | author = Fedonkin, M. A.
 | year = 1992
 | title = Vendian faunas and the early evolution of Metazoa
 | pages = 87–129
 | url = https://books.google.com/books?id=gUQMKiJOj64C&pg=PP1
 | isbn = 978-0-306-44067-0
 | publisher = Springer
 | access-date = 2007-03-08
 }}</ref> Putative "burrows" dating as far back as {{Ma|1100|million&nbsp;years}} may have been made by animals that fed on the undersides of microbial mats, which would have shielded them from a chemically unpleasant ocean;<ref name=Seilacher1998>{{cite journal
 | author = Seilacher, A.
 | author-link = Adolf Seilacher |author2=Bose, P. K. |author3=Pflüger, F.
 | date = 1998-10-02
 | title = Triploblastic Animals More Than 1 Billion Years Ago: Trace Fossil Evidence from India
 | journal = Science
 | volume = 282
 | issue = 5386
 | pages = 80–83
 | doi = 10.1126/science.282.5386.80
 | pmid = 9756480
 |bibcode = 1998Sci...282...80S }}</ref>
however, their uneven width and tapering ends make it difficult to believe that they were made by living organisms,<ref name=Budd2000>{{cite journal
 | author = Budd, G. E.
 |author2=Jensen, S.
 | year = 2000
 | title = A critical reappraisal of the fossil record of the bilaterian phyla
 | journal = Biological Reviews
 | volume = 75
 | issue = 2
 | pages = 253–295
 | doi = 10.1111/j.1469-185X.1999.tb00046.x
 | url = http://www.journals.cambridge.org/abstract_S000632310000548X 
 | access-date = 2007-06-27
 | format = abstract
| pmid=10881389|s2cid=39772232
 | url-access = subscription
 }}</ref> and the original author has suggested that the menisci of burst bubbles are more likely to have created the marks he observed.<ref>{{cite journal 
 | doi = 10.1126/science.1166220 
 | title = PALEONTOLOGY: Reading Behavior from the Rocks 
 | year = 2008 
 | author = Jensen, S.
 | journal = Science 
 | volume = 322 
 | pages = 1051–1052 
 | issue = 5904 | s2cid = 129734373 
 }}</ref>
The Ediacaran burrows found so far imply simple behaviour, and the complex, efficient feeding traces common from the start of the Cambrian are absent.

Some simple pre-Cambrian horizontal traces could have been produced by large single-celled organisms; equivalent traces are produced by protists today.<ref>{{cite journal| first1 = V. | first2 = M. | first3 = J. | first4 = A. | first5 = S.| title = Giant Deep-Sea Protist Produces Bilaterian-like Traces| last1 = Matz| last5 = Johnsen| last2 = Frank| last3 = Marshall| journal = Current Biology| volume = 18| issue = 23| pages = 1849–1854| date=Dec 2008 | issn = 0960-9822| pmid = 19026540| last4 = Widder| doi = 10.1016/j.cub.2008.10.028| s2cid = 8819675 | doi-access = free| bibcode = 2008CBio...18.1849M }}</ref>

==The early Cambrian diversification of burrow forms==

From the very start of the Cambrian period<ref name=Gehling2001/> (about {{Ma|538.8}})<ref name=LatestGTS>{{cite web|url=https://stratigraphy.org/chart#latest-version|title=Latest version of international chronostratigraphic chart|publisher=[[International Commission on Stratigraphy]]|lang=en|access-date=2024-04-07}}</ref> many new types of traces first appear, including well-known vertical burrows such as ''[[Diplocraterion]]'' and ''[[Skolithos]]'', and traces normally attributed to [[arthropod]]s, such as ''[[Cruziana]]'' and ''[[Rusophycus]]''. The vertical burrows indicate that worm-like animals acquired new behaviours, and possibly new physical capabilities. Some Cambrian trace fossils indicate that their makers possessed hard (although not necessarily mineralised<!--is "chitin" being avoided?-->) [[exoskeletons]].<ref name=Jensen2003>{{cite journal
| title=The Proterozoic and Earliest Cambrian Trace Fossil Record; Patterns, Problems and Perspectives
| author=Jensen, S.
| journal=Integrative and Comparative Biology
| doi = 10.1093/icb/43.1.219
| year=2003
| volume=43
| pages=219–28
| pmid=21680425
| issue=1| doi-access=free
}}</ref>

It's important to make a distinction between burrowing that introduces oxygen into the sediment – bioirrigation – and those that simply move sediment grains around – biomixing.  The latter can actually reduce the amount of oxygen available in the sediment, by bringing organic material down to depths where it will be anaerobically respired.  In ichnodiversity terms, the same proportions of these two modes (predominantly biomixing) are seen on each side of the Ediacaran-Cambrian boundary – even if bioirrigation occurrences become relatively more frequent in the Terreneuvian.<ref>{{Cite journal |author=Alison T. Cribb |author2=Sebastiaan J. van de Velde |author3=William M. Berelson |author4=David J. Bottjer |author5=Frank A. Corsetti |date=22 February 2023 |title=Ediacaran–Cambrian bioturbation did not extensively oxygenate sediments in shallow marine ecosystems |journal=Geobiology |volume=21 |issue=4 |pages=435–453 |type=Preprint |doi=10.1111/gbi.12550 |pmid=36815223 |bibcode=2023Gbio...21..435C |doi-access=free|hdl=2013/ULB-DIPOT:oai:dipot.ulb.ac.be:2013/356493 |hdl-access=free }}</ref>

==Advantages of burrowing==

===Feeding===
Many organisms burrow to obtain food, either in the form of other burrowing organisms, or organic matter.  The remains of planktonic organisms sink to the sea floor, providing a source of nutrition; if these organics are mixed into the sediment they can be fed upon.  However, it is possible that before the Cambrian, plankton were too small to sink, so there was no supply of organic carbon to the sea floor.<ref name=Butterfield2001>{{cite book|last1=Butterfield|first1=N. J.|chapter=Ecology and Evolution of Cambrian Plankton|title=The Ecology of the Cambrian Radiation|date=2000|editor1-last=Zhuravlev|editor1-first=A.|editor2-last=Riding|editor2-first=R.|pages=200–216|isbn=978-0-231-50516-1|doi=10.7312/zhur10612-009|publisher=Columbia University Press}}</ref>
However, it appears that organisms did not feed upon the sediment itself until after the Cambrian.<ref name="Butterfield200?"><!--I read this in a Butterfield paper today (1st July), but can't remember which one!!!  I'll hopefully come across it again presently. --></ref>

===Anchorage===
An advantage to living within the substrate would be protection from being washed away by currents.{{Verify source|date=July 2008}}

===Protection===

Organisms also burrow to avoid predation.  [[Predation#Evolutionary history|Predatory behaviour]] first appeared over 1 billion years ago, but predation on large organisms appears to have first become significant shortly before the start of the Cambrian.  Precambrian burrows served a protective function, as the animals that made them fed above the surface; they evolved at the same time as other organisms began forming mineralised skeletons.<ref name=Dzik2007/>

==Enabling burrowing==
Microbial mats formed a blanket, cutting off the underlying sediments from the ocean water above.  This meant that the sediments were [[Anoxic waters|anoxic]], and [[hydrogen sulfide]] ({{h2s}}) was abundant. The free exchange of the pore waters with oxygenated ocean water was essential to make the sediments habitable. This exchange was made possible by the action of minute animals: Too small to produce burrows of their own, this [[Fauna#Meiofauna|meiofauna]] inhabited the spaces between sand grains in the microbial mats. Their [[bioturbation]] – movement that dislodged grains and disturbed the resistant biomats – broke the mats up, allowing water and chemicals above and below to mix.<ref name=Seilacher2005/>

==Effects of the revolution==
The Cambrian substrate revolution was a long and patchy process that proceeded at different rates in different locations throughout much of the [[Cambrian]].<ref>{{cite journal
 |title        = Evidence for seafloor microbial mats and associated metazoan lifestyles in Lower Cambrian phosphorites of Southwest China
 |author1      = Dornbos, S.
 |author2      = Bottjer, D.
 |author3      = Chen, J.-Y.
 |journal      = Lethaia
 |issue        = 2
 |date         = June 2004
 |pages        = 127–137
 |doi          = 10.1080/00241160410004764
 |url          = http://www.uwm.edu/~sdornbos/PDF's/Dornbos%20et%20al.%202004.pdf
 |access-date   = 2008-08-04
 |volume       = 37
 |archive-url  = https://web.archive.org/web/20070106134133/http://www.uwm.edu/~sdornbos/PDF's/Dornbos%20et%20al.%202004.pdf
 |archive-date = 2007-01-06
 }}</ref>

===Effects on ecosystems===
After the agronomic revolution, the [[microbial mat]]s that had covered the Ediacaran sea floor became increasingly restricted to a limited range of environments:
*Very harsh environments, such as hyper-saline lagoons or brackish estuaries, which were uninhabitable for the burrowing organisms that broke up the mats.<ref name=Seilacher2005/>
*Rocky substrates which the burrowers could not penetrate.<ref name="BottjerEtAl2000CambrianSubstrateRevolution" />
*The depths of the oceans, where burrowing activity today is at a similar level to that in the shallow coastal seas before the revolution.<ref name="BottjerEtAl2000CambrianSubstrateRevolution" />
The first burrowers probably fed on the microbial mats, while burrowing underneath them for protection; this burrowing led to the downfall of the mats they were feeding on.<ref name=Dzik2007>{{The Rise and Fall of the Ediacaran Biota |author=Dzik, J |chapter=The Verdun Syndrome: simultaneous origin of protective armour and infaunal shelters at the Precambrian–Cambrian transition |pages=405–414 |doi=10.1144/SP286.30}}</ref>

Before the revolution, bottom dwelling organisms fell into four categories:<ref name="BottjerEtAl2000CambrianSubstrateRevolution" />
*"mat encrusters", which were permanently attached to the mat;
*"mat scratchers", which grazed the surface of the mat without destroying it;
*"mat stickers", suspension feeders that were partially embedded in the mat; and
*"undermat miners", which burrowed underneath the mat and fed on decomposing mat material.

The "undermat miners" appear to have died out by the middle of the [[Cambrian]] period.<ref name=Seilacher2005/> "Mat encrusters" and "mat stickers" either died out or developed more secure [[Holdfast (biology)|anchors]] that were specialised for soft or hard substrates. "Mat scratchers" were restricted to rocky substrates and the depths of the oceans, where both they and the mats could survive.<ref name="BottjerEtAl2000CambrianSubstrateRevolution" />
[[File:OrdCrinoidHoldfasts.jpg| thumb | right | 200px |[[Crinoid]] holdfasts on a hard substrate from the Upper [[Ordovician]] of northern Kentucky]]
Early [[Sessility (zoology)|sessile]] [[echinoderm]]s were mostly "mat stickers". The [[helicoplacus|helicoplacoids]] failed to adapt to the new conditions and died out; the [[edrioasteroids]] and [[eocrinoid]]s survived by developing holdfasts for attachment to hard substrates, and stalks that raised their feeding apparatus above most of the debris that burrowers stirred up in the looser sea-floors. Mobile echinoderms ([[stylophoran]]s, [[homostelean]]s, [[homoiostelean]]s, and [[ctenocystoid]]s) were not significantly affected by the substrate revolution.<ref name="BottjerEtAl2000CambrianSubstrateRevolution" />

Early [[mollusc]]s appear to have grazed on microbial mats, so it is natural to hypothesize that grazing molluscs were also restricted to areas where the mats could survive. The earliest known fossils of [[monoplacophora]]n ("single-plated") molluscs date from the Early Cambrian, where they grazed on microbial mats. Most modern monoplacophorans live on soft substrates in deep parts of the seas, although one [[genus]] lives on hard substrates at the edges of [[continental shelf|continental shelves]]. Unfortunately, the oldest known fossils of [[polyplacophora]]ns (molluscs with multiple shell plates) are from the Late Cambrian, when the substrate revolution had significantly changed marine environments. Since they are found with [[stromatolite]]s (stubby pillars built by some types of microbial mat colony), it is thought that polyplacophorans grazed on microbial mats. Modern polyplacophorans mainly graze on mats on rocky coastlines, although a few live in the deep sea.<ref name="BottjerEtAl2000CambrianSubstrateRevolution" /> No fossils have been found of [[aplacophora]]ns (shell-less molluscs), which are generally regarded as the most primitive living molluscs. Some burrow into the sea-floors of deep waters, feeding on micro-organisms and detritus; others live on reefs and eat coral polyps.<ref>{{cite web | url=http://www.ucmp.berkeley.edu/taxa/inverts/mollusca/aplacophora.php | title=The Aplacophora | publisher=University of California Museum of Paleontology | access-date=2008-07-03 }}</ref>

===Palaeontological significance===
The revolution put an end to the conditions which allowed [[Burgess Shale type preservation|exceptionally preserved]] fossil beds or ''[[lagerstätten]]'' such as the [[Burgess Shale]] to be formed.<ref name=Seilacher2005/> The direct consumption of carcasses was relatively unimportant in reducing fossilisation,  compared to changes in sediments' chemistry, porosity, and microbiology, which made it difficult for the chemical gradients necessary for soft-tissue mineralisation to develop.<ref name="Orr2003">{{cite journal | title=Post-Cambrian closure of the deep-water slope-basin taphonomic window | author=Orr, P.J. | author2=Benton, M.J. | author-link2=Michael Benton | author3=Briggs, D.E.G. | s2cid=129502810 | author-link3=Derek Briggs | year=2003 | doi=10.1130/G19193.1 | journal=Geology | volume=31 | pages=769 | bibcode=2003Geo....31..769O | issue=9 }}</ref>  Just like microbial mats, environments which could produce this mode of fossilisation became increasingly restricted to harsher and deeper areas, where burrowers could not establish a foothold; as time progressed, the extent of burrowing increased sufficiently to effectively make this mode of preservation impossible.<ref name=Orr2003/>  Post-Cambrian ''lagerstätten'' of this nature are typically found in very unusual environments.

The rise in burrowing is of further significance, for burrows provide firm evidence of complex organisms; they are also much more readily preserved than body fossils, to the extent that the absence of trace fossils has been used to imply the genuine absence of large, motile bottom-dwelling organisms.  This furthers palaeontologists' understanding of the early Cambrian, and provides an additional line of evidence to show that the [[Cambrian explosion]] represents a real diversification, and is not a preservational artefact - even if its timing did not coincide directly with the Agronomic revolution.<ref name=Seilacher2005/>

The rise of burrowing represents such a fundamental change to the [[Paleoecology|ecosystem]], that the appearance of the complex burrow ''[[Treptichnus pedum]]'' is used to mark the base of the Cambrian period.<ref name=Gehling2001>though it has since been found in lower, technically "Precambrian", strata.
*{{Cite journal| first1 = J.| first2 = S. R.| last2 = Jensen | first3 = M.| last4 = Myrow| last3 = Droser| last5 = Narbonne| first4 = P.| first5 = G.  | title = Burrowing below the basal Cambrian GSSP, Fortune Head, Newfoundland  | journal = Geological Magazine  | volume = 138  | issue = 2  | pages = 213–218  | date=March 2001 | last1 = Gehling  | doi = 10.1017/S001675680100509X| bibcode = 2001GeoM..138..213G| hdl = 10662/24314| s2cid = 131211543| hdl-access = free}}</ref>

===Geochemical significance===

The increased level of bioturbation meant that sulfur, which is steadily supplied to the oceanic system from volcanoes and river runoff, was more readily oxidised - rather than being rapidly buried and sitting in its reduced form (sulfide), burrowing organisms continually exposed it to oxygen, allowing it to be oxidised to sulfate.   This activity is suggested to account for a sudden rise in sulfate concentration observed near the base of the Cambrian; this can be recorded in the geochemical record both by using {{delta|34|S|link}} isotopic tracers, and by quantifying the abundance of the sulfate mineral [[gypsum]].<ref name=Canfield2009>{{Cite journal| first1 = E. | first2=J.| title = Animal evolution, bioturbation, and the sulfate concentration of the oceans| journal = Proceedings of the National Academy of Sciences of the United States of America| last2= Farquhar| volume = 106| issue = 20| pages = 8123–8127| date=May 2009 | issn = 0027-8424| pmid = 19451639| last1 = Canfield| pmc = 2688866| doi = 10.1073/pnas.0902037106|bibcode = 2009PNAS..106.8123C | doi-access=free}}</ref>

==See also==
*[[Matground]]

==Further reading==
{{Cite journal| first1 = R. H. T.| last1 = Callow | first2 = M. D.| title = Remarkable preservation of microbial mats in Neoproterozoic siliciclastic settings: Implications for Ediacaran taphonomic models| journal = Earth-Science Reviews| volume = 96| issue = 3| pages = 207–219| year = 2009| doi = 10.1016/j.earscirev.2009.07.002| last2 =  Brasier|bibcode = 2009ESRv...96..207C | citeseerx = 10.1.1.426.2250 }}

==References==
{{Reflist}}
*{{cite journal|url=https://www.sciencedirect.com/science/article/abs/pii/S0031018207004543|title= The importance of Planolites in the Cambrian substrate revolution|year= 2008|doi= 10.1016/j.palaeo.2007.05.025|last1= Marenco|first1= Katherine N.|last2= Bottjer|first2= David J.|journal= Palaeogeography, Palaeoclimatology, Palaeoecology|volume= 258|issue= 3|pages= 189–199|bibcode= 2008PPP...258..189M|url-access= subscription}}
*{{cite journal|title=The Cambrian substrate revolution and early evolution of the phyla|year=2010 |doi=10.1007/s12583-010-0160-7 |last1=Bottjer |first1=David J. |journal=Journal of Earth Science |volume=21 |issue=S1 |pages=21–24 |bibcode=2010JEaSc..21S..21B |s2cid=129851901 }}
*{{cite journal|url=https://pubs.geoscienceworld.org/gsa/geology/article-abstract/28/9/839/188912/Evolutionary-paleoecology-of-the-earliest?redirectedFrom=fulltext|title= Evolutionary paleoecology of the earliest echinoderms: Helicoplacoids and the Cambrian substrate revolution|bibcode= 2000Geo....28..839D|last1= Dornbos|first1= Stephen Q.|last2= Bottjer|first2= David J.|journal= Geology|year= 2000|volume= 28|issue= 9|page= 839|doi= 10.1130/0091-7613(2000)28<839:EPOTEE>2.0.CO;2|url-access= subscription}}

[[Category:Cambrian]]