Marine oxygenation, lithistid sponges, and the early ......Cambrian, and why did it take so long for the bryozoan-coral-stroma-toporoid community to emerge in the Ordovician? Explanations

Contents lists available at ScienceDirect

Earth-Science Reviews

journal homepage wwwelseviercomlocateearscirev

Marine oxygenation lithistid sponges and the early history of Paleozoicskeletal reefs

Jeong-Hyun Leea Robert Ridingb

a Department of Geology and Earth Environmental Sciences Chungnam National University Daejeon 34134 Republic of KoreabDepartment of Earth and Planetary Sciences University of Tennessee Knoxville TN 37996 USA

A R T I C L E I N F O

KeywordsCambrianReef gapDysoxiaHypoxiaLithistid sponge-microbial reef

A B S T R A C T

Microbial carbonates were major components of early Paleozoic reefs until coral-stromatoporoid-bryozoan reefsappeared in the mid-Ordovician Microbial reefs were augmented by archaeocyath sponges for ~15Myr in theearly Cambrian by lithistid sponges for the remaining ~25Myr of the Cambrian and then by lithistid calathiidand pulchrilaminid sponges for the first ~25Myr of the Ordovician The factors responsible for midndashlateCambrian microbial-lithistid sponge reef dominance remain unclear Although oxygen increase appears to havesignificantly contributed to the early Cambrian lsquoExplosionrsquo of marine animal life it was followed by a prolongedperiod dominated by lsquogreenhousersquo conditions as sea-level rose and CO2 increased The midndashlate Cambrian wasunusually warm and these elevated temperatures can be expected to have lowered oxygen solubility and tohave promoted widespread thermal stratification resulting in marine dysoxia and hypoxia Greenhouse condi-tions would also have stimulated carbonate platform development locally further limiting shallow-water cir-culation Low marine oxygenation has been linked to episodic extinctions of phytoplankton trilobites and othermetazoans during the midndashlate Cambrian We propose that this tendency to dysoxia-hypoxia in shallow marineenvironments also limited many metazoan reef-builders In contrast during the midndashlate Cambrian the ability oflithistid sponges to withstand low oxygen levels allowed them to create a benthic association with microbialcarbonates that dominated global reefs These conditions ameliorated during the Ordovician as temperaturedecline promoted ocean ventilation The prolonged time gap occupied by low diversity reefs between thelsquoCambrian Explosionrsquo and the lsquoGreat Ordovician Biodiversification Eventrsquo reflects elevated temperatures andreduced marine oxygenation that limited metazoan diversification in shallow marine environments

1 Introduction

The early Paleozoic radiation of marine animals commonly referredto as the lsquoCambrian Explosionrsquo (Cloud 1948 Bowring et al 1993Conway Morris 2006) stalled in the mid-Cambrian and did not regainimpetus until the mid-Ordovician (Sepkoski Jr 1981 Webby 2002Bambach et al 2004) during the lsquoGreat Ordovician BiodiversitificationEventrsquo (Webby et al 2004) Reef development shows a similar patternleading to the observation that midndashlate Cambrian reef communitieswere dominantly microbial (Fagerstrom 1987 Zhuravlev 1996Rowland and Shapiro 2002) As a result the prolonged interval be-tween late early Cambrian extinction of archaeocyath sponges and theEarly Ordovician rise of lithistid sponge-microbial-calathiid reef com-munities came to be regarded as a ldquoreef gaprdquo (Sheehan 1985Zhuravlev 1996 Rowland and Shapiro 2002 Kiessling 2009) Chal-lenges to this view first emerged in the report of early Furongian (lateCambrian) lithistid sponge-microbial (LSM) reefs in Iran (Hamdi et al

1995) Additional examples of midndashlate Cambrian LSM reefs have sincebeen recognized throughout Laurentia and Gondwana (Mrozek et al2003 Shapiro and Rigby 2004 Johns et al 2007 Kruse andZhuravlev 2008 Hong et al 2012 2016 Kruse and Reitner 2014Adachi et al 2015 Lee et al 2016a) It is now clear that LSM reefcommunities were globally distributed for ~25Myr during the midndashlateCambrian This community was augmented in the Early Ordovician by avariety of skeletal organisms such as Calathium Pulchrilamina Am-sassia bryozoans stromatoporoids and Lichenaria but reef diversifi-cation remained relatively slow until bryozoans corals and stromato-poroids became common in the mid-Ordovician ~460Ma (Fagerstrom1987 Webby 2002 Servais et al 2009) Numerical ages used hereaccord with those of the International Chronostratigraphic Chart(Cohen et al 2013) Recognition of midndashlate Cambrian LSM reefscloses the ldquoreef gaprdquo (Lee et al 2016a and references therein) but alsoraises questions What factors contributed to lithistid success followingarchaeocyath decline why did LSM reefs dominate the remainder of the

httpsdoiorg101016jearscirev201804003Received 13 January 2018 Received in revised form 6 April 2018 Accepted 6 April 2018

Corresponding authorE-mail addresses jeonghyunleecnuackr (J-H Lee) rridingutkedu (R Riding)

Earth-Science Reviews 181 (2018) 98ndash121

Cambrian and why did it take so long for the bryozoan-coral-stroma-toporoid community to emerge in the Ordovician Explanations forthese aspects of reef developments could shed light on broader patternsof change that continue to be debated particularly the seemingly slowoverall pace of midndashlate Cambrian animal diversification (Sepkoski Jr1981 Pruss et al 2010 Knoll and Fischer 2011 McKenzie et al 2014Saltzman et al 2015)

Here we explore the possibility that prolonged low levels of marineoxygenation significantly influenced the relative success and develop-ment of reef communities during the midndashlate Cambrian and EarlyOrdovician (Webby 2002 Saltzman et al 2015 Lee and Riding2016) High midndashlate Cambrian sea-level and elevated atmospheric CO2

promoted lsquogreenhousersquo conditions with elevated temperatures (Berner1990 2009 McKenzie et al 2014) Higher temperatures decreaseoxygen solubility in seawater increase thermal stratification of theocean and favor marine productivity while simultaneously stimulatingcarbonate platform development that restricts shallow-water circula-tion Collectively these factors tend to induce episodic marine dysoxia-hypoxia (Saltzman 2005 Gill et al 2011) that has been linked to re-peated extinctions of phytoplankton trilobites and other metazoansduring the midndashlate Cambrian (eg Bambach et al 2004)

We propose that lithistid sponges along with microbes were pre-disposed to tolerate low oxygen levels and that this was a central factorin their development and persistence during the midndashlate CambrianThese conditions began to change in the Early Ordovician as tempera-ture decline (Trotter et al 2008) promoted ocean ventilation(Thompson et al 2012 Kah et al 2016 Young et al 2016) In themid-Ordovician the bryozoan-coral-stromatoporoid community estab-lished itself as the next major phase of Paleozoic reef development(Pitcher 1964 Fagerstrom 1987) From this perspective the re-lationship between reef community evolution and dysoxia-hypoxia is akey to understanding not only the Cambrian ldquoreef gaprdquo but also therelatively slow progress of animal radiation in mid-Cambrian to mid-Ordovician shallow marine environments

2 CambrianndashOrdovician marine diversity

Marine animal generic diversity shows a plateau in the lateCambrian (Furongian Epoch Paibian and Jiangshanian ages)(~510ndash485Ma) (Sepkoski Jr 1979 1981) before recovering near theCambrianndashOrdovician transition (Na and Kiessling 2015) This intervalof depressed diversity largely reflects archaeocyath extinctions fol-lowed by trilobite extinctions and low levels of origination (Bambachet al 2004) Midndashlate Cambrian and Early Ordovician trilobite ex-tinctions define ldquobiomererdquo boundaries (Palmer 1984 Taylor 2006)that as in the case of the late Cambrian Age 3 Sinsk Event (Zhuravlevand Wood 1996) have been linked to influxes of anoxic andor coldbasinal waters onto shallow shelves (Stitt 1975 Palmer 1984 Westropand Ludvigsen 1987) This is consistent with survival of trilobitesadapted to reduced oxygen availability at biomere boundaries (Palmer1984 Taylor 2006 McKenzie et al 2014 Saltzman et al 2015) Inaddition dysoxia-tolerant arthropod groups such as olenids (Fortey2000) and phosphatocopids (Williams et al 2011) increased in di-versity in the late Cambrian (Fig 1)

Biomere and other Cambrian biotic turnoversextinctions have inturn been linked to carbon isotope excursions (Taylor 2006 Zhu et al2006 Peng et al 2012 Saltzman et al 2015) In addition to the~510Ma Sinsk Event these include the early Paibian Marju-miidndashPterocephaliid biomere boundary and the early JiangshanianPterocephaliidndashPtychaspid biomere boundary which approximatelycorrespond with the lower and upper boundaries respectively of theSteptoean positive carbon isotope excursion (SPICE) event (Saltzmanet al 1995 2000 Perfetta et al 1999 Saltzman 1999 Montantildeezet al 2000 Lee et al 2015a Gerhardt and Gill 2016) (for correlationssee Taylor et al 2012 fig 1) (Fig 1) We infer along with others thatmidndashlate Cambrian extinctions occurred as poorly oxygenated basinal

water encroached onto carbonate platforms stressing shallow-watercommunities (Palmer 1984 Berry et al 1989 Taylor 2006 Gill et al2011 Landing 2012a 2012b Saltzman et al 2015) Similar effectshave been invoked to account for extinction of carbonate platformcommunities in JurassicndashCretaceous Oceanic Anoxic Events (Schlangerand Jenkyns 1976 Jenkyns 1991 2010 Parente et al 2008)

Marine diversity greatly increased during the Ordovician (SepkoskiJr 1981) The Great Ordovician Biodiversification Event (GOBE)(Webby et al 2004) was a diachronous and extended event initiated inthe Furongian and accelerating in the Darriwilian that continued untilalmost the end of the Ordovician (Sepkoski Jr 1981 Webby et al2004 Harper 2006 Servais et al 2010 2016) Significant increases inanimal biodiversity at family genus and species level resulted in therise of the lsquoPaleozoic Evolutionary Faunarsquo dominated by suspension-feeding organisms such as brachiopods rugose and tabulate coralscrinoids bryozoans and stromatoporoids (Sepkoski Jr 1979 Bambachet al 2002) This community developed throughout the Early Ordo-vician and by the late Darriwilian had a radical affect on reef building(Pitcher 1964 Fagerstrom 1987 Webby 2002 Webby et al 2004) Inaddition global increase in phytoplankton (acritarch) diversity broadlyparalleling that of animals occurred in the Furongian and Early Or-dovician (Servais et al 2008 2016 Nowak et al 2015) These Or-dovician upturns in diversity have been broadly related to increase inatmospheric O2 (Servais et al 2008 2010 2016 Saltzman et al 2011Edwards et al 2017) and decline in global temperature (Trotter et al2008)

3 Late Ediacaranndashmid-Ordovician eukaryote reef development

Microbial carbonates (stromatolites thrombolites and associated calci-microbes) generally dominated reefs from the Ediacaran to the EarlyOrdovician The earliest skeletal reefs involved Ediacaran calcified sessilebenthic eukaryotes (Cloudina Namacalathus Namapoikia) and earlyCambrian ldquoLadathecardquo Archaeocyaths and locally radiocyaths and cor-alomorphs are conspicuous in early Cambrian reefs Archaeocyaths andcoralomorphs continued ndash although much reduced ndash during the midndashlateCambrian when lithistid sponges were the most prominent components ofskeletal reefs Large lithistids (Archaeoscyphia) appeared in the EarlyOrdovician augmented by calathiids pulchrilaminids and the first un-disputed tabulate corals bryozoans and stromatoporoids These latter ap-pearances set the scene for the mid-Ordovician diversification of stroma-toporoids tabulates and bryozoans that created reefs dominated byencrusting and massive skeletons at the end of the Darriwilian

The affinities of many EdiacaranndashOrdovician skeletons remainproblematic Namapoikia may be a chaetetid sponge or simple colonialcnidarian (Wood et al 2002 Wood 2017) Archaeocyaths and lithis-tids are sponges Radiocyath skeletal structure resembles that of Ca-lathium which is sponge-like (Church 1991 Rowland 2001) and alsothat of cyclocrinitids (Beadle 1988) but these groups have also beencompared with green algae (eg Nitecki and Debrenne 1979) Cor-alomorphs comprise a heterogeneous semi-formal group encompassingmassive as well as cuplike skeletons some of them are considered realcorals (eg Scrutton 1997 Hicks 2006) Pulchrilaminids are stroma-toporoid-like but regarded as a separate group of hypercalcifiedsponges (Webby 2015)

Based on their eukaryote skeletal components we distinguish six reefintervals during this ~100Myr period (~550ndash444Ma) when reefs evolvedfrom mainly microbial into mainly skeletal structures Time scales are basedon Peng et al (2012) Cohen et al (2013) and Ogg et al (2016) These mainreef intervals are I late Ediacaran (~550ndash541Ma) microbial-Cloudina IIFortunianndashmid-Age 2 (541ndash525Ma) microbial-ldquoLadathecardquo III mid-Age 2late Age 4 (525ndash510Ma) microbial-archaeocyath IV late Age 4end Age 10(510ndash485Ma) microbial-lithistid V Tremadocianndashmiddle Darriwilian(485ndash460Ma) microbial-lithistid-calathiid-pulchrilaminid VI late Darriwi-lianndashend-Ordovician (460Mandash444Ma) stromatoporoid-bryozoan-tabulate-receptaculitid-microbial

J-H Lee R Riding Earth-Science Reviews 181 (2018) 98ndash121

31 Late Ediacaran (~550ndash541 Ma) microbial-Cloudina

Calcified sessile problematic metazoans contributed to and locallyconstructed reefs in the late Ediacaran (~550ndash541Ma) (Germs 1972Conway Morris et al 1990 Seilacher 1999 Grotzinger et al 2000Hofmann and Mountjoy 2001 Penny et al 2014 2017 Wood 2017)Masses of narrow conical calcified Cloudina tubes (annelid or cnidarianVinn and Zatoń 2012 Pacheco et al 2015) individually up to 8mmwide and 15 cm long constructed reefs up to 7m wide and 3m high(Wood 2017) Cloudina also often occurs in stromatolite and throm-bolite reefs locally in association with stalked cups of the calcified but

very thin-walled problematic Namacalathus (lophophorate Zhuravlevet al 2015) up to 35mm in size (Grotzinger et al 2000 Hofmann andMountjoy 2001 Zhuravlev et al 2015 Wood 2017) Cloudina andNamacalathus locally mutually attached (Penny et al 2014 2017)Namapoikia another early metazoan in late Ediacaran microbial reefsis tabular crustose and chaetetid-like (see 334 Chaetetids below)(Wood et al 2002) composed of millimetric labyrinthine tubules andin cavities locally forms sheet-like crusts up to 1m in extent (Wood2017) Cloudina Namacalathus and Namapoikia are not known to havesurvived into the Cambrian (Amthor et al 2003)

Generic diversity of calcifying animals Phosphatocopid

genera

Dysoxia-tolerant arthropods Anoxic events

Extinctionevents

Blackshales

Oxygentrends

Green Point

Global ocean deoxygenation

Atmospheric oxygen concentrations

lation

l- lith

isti d

Hawkersquos Bay event

end-Marjumiid

end-Pterocephaliid

end-Ptychaspid

end-Skullockianend-Stairsian

Cambrian-Ordovician

Redlichiid-Olenellid

archaeocyath and trilobite

0Olenid species

Early Darriwilian global ocean ventilation

0 100 0 10

Fig 1 Cambrian to Middle Ordovician oxygen level indicators and associated changes in biotic diversity Generic diversity of calcifying animal groups (AnthozoaArchaeocyathida Articulata Bryozoa Demospongia Echinodermata Mollusca Ostracoda and Trilobita) after Pruss et al (2010) Olenid trilobite diversity fromhttpfossilworksorg (accessed 22nd Dec 2017) Bivalved arthropod phosphatocopid diversity from Williams et al (2011) Extinction events adapted from 1Zhuravlev and Wood (1996) 2 Palmer and James (1979) 3 Peng et al (2012) 4 Palmer (1984) 5 Loch et al (1993) 6 Adrain et al (2009) Examples of blackshale deposits from Babcock et al (2015) 1 Pestrotsvet Fm Russia 2 Spence Shale Utah and Idaho USA 3 Burgess Shale British Columbia Canada 4 NiutitangFm South China 5 Alum Shale Scandinavia 6 Huaqiao Fm South China 7 White-leaved Oak Shale England Global anoxic events 1 Sinsk (Zhuravlev andWood 1996) 2 Redlichiid-Olenellid Extinction Carbon isotope Excursion (ROECE) (Zhu et al 2006 Faggetter et al 2017) 3 Steptoean Positive Carbon IsotopeExcursion (SPICE) (Saltzman et al 2000) 4 Reducing condition across the Cambro-Ordovician boundary at Green Point GSSP section (Tripathy et al 2014)Oxygenation trends 1 Global ocean oxygenation across the EdiacaranndashCambrian boundary indicated by Mo isotopes (Chen et al 2015) 2 Global ocean deox-ygenation indicated by bioturbation Mo isotopes TOC and U (Boyle et al 2014) 3 Atmospheric oxygen levels calculated by Edwards et al (2017) 4 Ordoviciansea-surface temperatures based on conodont thermometry (Trotter et al 2008) 5 Tremadocian-Floian ocean oxygenation (Saltzman et al 2015) 6 Early Darri-wilian global ocean ventilation (Kah et al 2016)

32 Earliest Cambrian Fortunianmid-Age 2 (541ndash525 Ma) microbial-ldquoLadathecardquo

Early Cambrian (Terreneuvian) reefs like those of the Ediacaranare predominantly stromatolitic and calcimicrobial (Drosdova 1980Riding and Voronova 1984 Kruse et al 1996) Among the shellyfossils that appeared in the Fortunian (Bengston 2004) a single ex-ample of a lsquoworm reefrsquo formed by operculate tubular ldquoLadathecardquo in-dividually up to 15 cm long and 6mm wide occurs in the late Fortunian(Landing 1993) and is reminiscent of Cloudina reefs

33 Early Cambrian mid-Age 2late Age 4 (525ndash510 Ma) microbial-archaeocyath

331 ArchaeocyathsArchaeocyaths previously considered a distinct phylum or com-

pared with coelenterates and algae are now regarded as sponges(Debrenne et al 2015b) These distinctive and often heavily calcifiedskeletons typically conical with porous walls partitioned and supportedby septa appeared in the lower Tommotian Stage of Siberia (mid-Age 2~525Ma Ogg et al 2016) in the zone named after the archaeocyathNochoroicyathus sunnaginicus (Fig 2) Most archaeocyath cups arelt15mm in diameter and several centimeters in height but examples15 m in size are reported and some show mutual attachment that fa-vored reef-construction (Hill 1964 Wood et al 1993 Debrenne et al2015b) They were long regarded as the first animals to attain a globalreef-building role (Fagerstrom 1987 Rowland and Gangloff 1988Wood 1999 Knoll 2003 Gandin and Debrenne 2010) and some early

Cambrian reefs are dominated by archaeocyath frameworks (Rowland1984 Riding and Zhuravlev 1995) However they are usually alsoclosely associated with abundant calcimicrobes (Pratt et al 2001Riding 2001 Lee et al 2014b) that diversified in the early Cambrian(Riding and Voronova 1984 Zhuravlev 1996) and less commonlywith coralomorphs and radiocyaths (Jell 1984 Kruse et al 19951996 Zhuravlev and Wood 1995 Zhuravlev 2001a Zhuravlev et al2015) (Fig 3) The peak of archaeocyath diversity in Age 3 (~518Ma)coincided with that of marine animal genera as a whole (Na andKiessling 2015) but the group declined rapidly ~510Ma (Peng et al2012) Archaeocyath decline sometimes considered the first significantextinction of the Phanerozoic (Newell 1972 Signor 1992 Zhuravlev1996 2001a Bambach et al 2002 Bambach 2006) was linked to theHawkes Bay Regression in the lower Toyonian Stage of Siberia (middleAge 4) by Palmer and James (1979) but Zhuravlev and Wood (1996)suggested that the anoxic Sinsk Event in the Botomian Stage of Siberia(late Age 3) may have been more important in reducing archaeocyathdiversity Hyoliths inarticulate brachiopods and trilobites also showreduced levels of originations in the Botomian (Bambach et al 2004)(Fig 1)

332 Cribricyaths radiocyathsDuring Cambrian Epoch 2 the diverse archaeocyath reef commu-

nity was augmented by other mostly problematic calcified skeletalorganisms of various shapes and sizes such as cribricyaths radiocyathsand coralomorphs Cribricyatha (Vologdin 1961) are small (lt 1 cmlong) locally abundant calcareous conical Problematica (Zhuravlev2001b) that contributed to reef formation (Wood et al 1993) in the

Pseudostylodictyon

Namacalathus

lsquoLadathecarsquo

Nochoroicyathus

Gonamispongia

Leibaella

Rankenella

Wilbernicyathus

Notch Peak

Calathium

Cyclocrinites

problematicum

archaeocyathradiocyathcysticyath

lithistid

pulchrilaminid

coralomorphchaetetidtabulate

NamapoikeaCysticyathus

HarklessiaFlindersipora Cambrotrypa

Cambroctoconus

Cambrophyllum

Lichenaria

Amsassia

Pulchrilamina

CystostromaSolenopora

Zondarella

Cloudina

Billingsaria

Pseudostylodictyon

bryozoan

Prophyllodictya

Nekhorosheviella Batostoma

4438 Ma

Late Ordovician

microbial-archaeocyath microbial-lithistid-calathiid-pulchrilaminidmicrobial-lithistid

Terreneuvian~521 ~509 ~497 4854

Furongian Early Ordovician541 470

Ediacaran

microbial-Cloudina

Middle Ordovician

microbial-Ladatheca stromatoporoid-bryozoan-tabulate-receptaculitid-microbial

stromatoporoid

receptaculitidcyclocrinitid

Epoch 2 Epoch 3

Fig 2 Schematic size shape and age summary of reef-building skeletal organisms from late Ediacaran to early Late Ordovician Time scales from Peng et al (2012)Cohen et al (2013) and Ogg et al (2016) Six reef intervals are recognized I Late Ediacaran (~550ndash541Ma) microbial reefs with Cloudina Namacalathus andNamapoikia II Earliest Cambrian (Fortunianndashmid-Age 2) microbial reefs with rare ldquoLadathecardquo III Microbial-archaeocyath sponge reefs with radiocyaths cor-alomorphs etc from mid-Age 2 to Age 4 IV Microbial-lithistid sponge reefs in the midndashlate Cambrian V Microbial-lithistid sponge reefs augmented by Calathiumpulchrilaminids bryozoans Lichenaria Amsassia and Cystostroma in the Early and early Middle Ordovician VI Skeletal-dominant reefs mainly constructed bystromatoporoids corals and bryozoans together with microbial carbonates in the late Darriwilian and Late Ordovician

early Cambrian (TommotianndashBotomian) (Debrenne et al 2015a) Anearly cribricyath is Leibaella (late Tommotian late Age 2) (Wood et al1993) Radiocyaths are similar in size and shape to archaeocyaths withwhich they were often confused (Kruse et al 2015) but were dis-tinguished as a distinct group (Radiocyatha) by Debrenne et al (1970)An early example is Gonamispongia (late Tommotian late Age 2)Radiocyaths have globular to pear-shaped skeletons with outer wallscomposed of distinctive plates (nesasters) and more closely resemblereceptaculitids than archaeocyaths (Nitecki and Debrenne 1979) al-though receptaculitids are not common until the Ordovician (seeSection 351 Receptaculitids radiocyaths cyclocrinitids below)However the largest skeletal additions to early Cambrian reef com-munities were locally made by coralomorphs such as Flindersipora(Fuller and Jenkins 2007)

333 Early Cambrian coralomorphsTabulate-like phosphatic fossils (eg Ramitubus) occur in the mid-

Ediacaran (~585Ma) Doushantuo Formation (Van Iten et al 2014)and Namapoikia may be a cnidarian (Wood et al 2002) Coral-likecalcified fossils are diverse in the early Cambrian (Zhuravlev et al1993 Wrona and Zhuravlev 1996 Scrutton 1999 Debrenne andReitner 2001 Hicks 2006 Fuller and Jenkins 2007) but are difficultto relate to Tabulata or Rugosa neither of which is confidently re-cognized until the Ordovician (Scrutton 1992 Oliver 1996 Scrutton1997) Jell (1984) placed coral-like early Cambrian fossils within theCoralomorpha This highly heterogeneous semi-formal group en-compasses chaetetids and early ldquotabulatesrdquo with or without septa andtabulae as well as cuplike skeletons

Early coralomorphs are best known from calcimicrobial-archae-ocyath reefs in the early Cambrian They exhibit two contrasting mor-photypes small cup-like and large massive domical Scrutton (1997)recognized two orders of Cambrian zoantharian corals (TabulaconidaDebrenne et al 1987 Cothoniida Oliver and Coates 1987) and sug-gested that calcified earlyndashearly middle Cambrian corals represent lsquoaseries of short-lived calcification episodes among contemporary ane-monesrsquo (Scrutton 1999) Middle Tommotian (523Ma) Cysticyathuspreviously included in archaeocyaths is an early cup-like coralomorphin calcimicrobial-archaeocyath reefs (Debrenne and Reitner 2001 fig146b) Somewhat younger cup-like forms include Age 5ndashDrumian

Cambroctoconus (Park et al 2011 Peel 2017b) Age 4 Cothonion (Peel2011) and Lipopora (see Park et al 2016) Some of these formed mid-Cambrian reefs eg Cambroctoconus (Lee et al 2016a) which hasbeen described as a stem-group cnidarian based on its octoradial sym-metry (Park et al 2011)

Much larger domical forms in the late Botomian (~513Ma) includeFlindersipora (Lafuste et al 1991 Savarese et al 1993 Debrenne andReitner 2001 Fuller and Jenkins 2007) Yaworipora (Zhuravlev1999) Moorowipora (Sorauf and Savarese 1995) Arrowipora andBlinmanipora (Scrutton 1992 1997 Fuller and Jenkins 2007) Flin-dersipora is up to 70 cm tall (Fuller and Jenkins 2007) Moorowiporaand Arrowipora cerioid forms with short septal spines and tabulaeresemble tabulates (Fuller and Jenkins 1994 1995 Sorauf andSavarese 1995) Contemporaneous Harklessia (BotomianndashToyo-nian=~5125Ma) lacks both septa and tabulae (Hicks 2006) Thesedomical coralomorphs declined at the end-early Cambrian and only afew middle and late Cambrian examples are known (Debrenne andReitner 2001)

334 ChaetetidsIn addition to coralomorphs modular calcified skeletons occur in

chaetetid sponges In general chaetetids have tabulae but poorly de-veloped - or no - septa whereas tabulate corals possess tabulae and mayor may not have well-developed septa (Scrutton 1979 1997 West2012) Ediacaran Namapoikia has been compared with both chaetetidsand coralomorphs (Wood et al 2002) Botomian Labyrinthus (Kobluk1979) and Rosellatana (Kobluk 1984) which attached to archae-ocyaths were regarded as coralomorphs by Debrenne and Reitner(2001) However their mode of increase similar to longitudinal fissionsuggests affinities with chaetetids more than corals (Scrutton 1997Pratt et al 2001) Cambrophyllum (Fritz and Howell 1955) from thelower Dresbachian Stage of North America (Guzhangian Age~499Ma) 30mm wide and 15mm high with septa-like processeswithin the lsquocorallitesrsquo (Scrutton 1979 Jell 1984 Kobluk 1984) hasalso been compared with chaetetids (Scrutton 1997) Solenopora(Riding 2004) first known in the early Darriwilian (~465Ma) (Klappaand James 1980) and common in the late Darriwilian (Kroumlger et al2017) and early Late Ordovician (Opalinski and Harland 1981) maybe the first abundant rock-forming chaetetid

~521 ~509 ~497 485

Tremadocian FloianAge

Legend

Lithistid sponge

Sediment within spongocoels

Microstromatoliteamp other microbial carbonate

Calcimicrobe(eg Epiphyton)

Sediment

Archaeocyath

Calathium

Cnidarian(+coralomorph) Pulchrilaminid

Pelmatozoan

Bryozoan

Relative proportion of reef-building components

Radiocyath

~529 470 Ma

Zhangxia FmRanken Lm Deh-Molla Fm

Notch Peak Fm

Sponge (other)

Early Ordovician

Drumian Pai-bian

Jiang-shanian

Guzhan-gian Age 10Age 5Age 4Age 3Age 2

Terreneuvian Epoch 2 Epoch 3 Furongian

Fig 3 Relative proportions of main reef components during the Cambrian and Early Ordovician Early Cambrian microbial-archaeocyath reefs from Gandin andDebrenne (2010) Early Ordovician microbial-lithistid-calathiid reefs from Hong et al (2015) Li et al (2015) and references therein Proportions of midndashlateCambrian reef-building components based on examples in Table 1

335 PelmatozoansPelmatozoans (stem-bearing echinoderms) appear in Cambrian

Epoch 2 (Zamora et al 2013 Peel 2017a) The eocrinoid Kinzercystisfrom early Epoch 2 (~519Ma) is an early example (Zamora et al 2013fig 133) Echinoderms declined in the GuzhangianndashPaibian and thenrecovered in the midndashlate Furongian (Zamora et al 2013) Echino-derms attached to firm substrates in the midndashlate Cambrian (Brett et al1983 Zamora et al 2010 2017) but within Cambrian reefs theymostly occur as scattered fragments (James and Kobluk 1978 Prussand Knoll 2017) and may have been passive filter feeders restricted tolow-velocity currents (Smith 1990) Only locally did they form reeffabric eg in the basal parts of some late Cambrian LSM reefs (Spincer1996 Johns et al 2007) Nonetheless together with bryozoans theirholdfasts created reef substrates in the late Tremadocian (~480Ma)(Adachi et al 2011 fig 6) Darriwilian (Pratt 1989) and Late Ordo-vician (eg Hemicosmites Kroumlger et al 2014)

34 Midndashlate Cambrian (ldquoreef gaprdquo) late Age 4end Age 10(510ndash485Ma) microbial-lithistid

Midndashlate Cambrian reefs have long been known to be dominantlymicrobial (Fagerstrom 1987 Rowland and Shapiro 2002 Riding2006) Lithistid sponges had been recognized in the midndashlate Cambrianbut were often considered too small too simple and too scarce to beeffective reef-builders (Fagerstrom 1987 Pratt et al 2001 Rowlandand Shapiro 2002) Consequently the interval between archaeocyathdecline at the end of the early Cambrian and the appearance of largeskeletal reefs in the mid-Ordovician came to be regarded as a majorlsquoreef gaprsquo the longest of the Phanerozoic (Copper 2001 Stanley 2001Rowland and Shapiro 2002 Kiessling 2009 James and Wood 2010)This view also tended to overlook the Early Ordovician reefs docu-mented by Toomey (1970) Copper (1974) Toomey and Nitecki (1979)and others that contain large domes and columns of Pulchrilamina aswell as conspicuous conical lithistids (Archaeoscyphia) and calathiids(Calathium) Lithistid sponges as a whole constitute a long-rangingpolyphyletic group of calcified demosponges (Pisera 2002 Pisera andLeacutevi 2002 Morrow and Caacuterdenas 2015 Schuster et al 2015) andcontinue to build reefs at the present-day (Maldonado et al 2015) Allknown Cambrian lithistids however belong to the Family Anthaspi-dellidae characterized by conical morphology and a distinctive lad-derlike spicule structure In overall shape and size anthaspidellidsbroadly resemble archaeocyaths and this similarity can extend to theirreef-building role (Hong et al 2016 Lee et al 2016a) Both arecommonly closely associated with and volumetrically subordinate tocalcimicrobes and other microbial carbonates in reefs (Kruse andZhuravlev 2008 Kruse and Reitner 2014 Adachi et al 2015 Leeet al 2016a)

For 25Myr throughout the midndashlate Cambrian skeletal reefs weredominated by cuplike lithistid sponges always in association with mi-crobial carbonates The earliest known lithistid is Rankenella from nearthe Age 45 boundary (Kruse 1983 1996) A series of studies begin-ning with Hamdi et al (1995) (Lee et al 2016a and references therein)(Fig 1 Table 1) recognized lithistid contributions to midndashlate Cam-brian reefs Lithistids were supported by their cemented basal attach-ments and interlocking spicules and they could develop external ridgedornamentation that may have increased nutrient intake (Church 2017)In Section 4 below we summarize well-described midndashlate Cambrianlithistid reefs and in Fig 2 show examples of lithistids In addition tolithistids midndashlate Cambrian reefs also locally contain abundant silic-eous sponges that have not yet been identified but appear to resemblekeratose sponges (cf Luo and Reitner 2014) and create maze-likeldquomaceriaterdquo structures (Lee et al 2014a 2015a 2016c Coulson andBrand 2016)

Most early Cambrian skeletal reef-builders declined in the midndashlateCambrian Radiocyaths disappeared in late Epoch 2 (middle Toyonian)(Kruse et al 2015) Archaeocyaths and coralomorphs declined Ta

ofmidndashlateCam

brianlithistid

icrobial

Location

Environm

Reefde

scription

Referen

ebulak

Lithistidspon

geOrlinocya

thus-Epiph

Teslen

ngProv

erStag

e5ndash

Shallow

subtidal

Lithistidspon

ankenella

)-calcim

icrobe

(Epiph

)-stem

-group

cnidarian(C

ambroctoconu

s)reefm

eter-scale

withinmicrobial-dom

treefframew

orkform

lattach

kenella

andCam

broctoconu

swithEp

encrustedby

microstromatolite

ietal(20

ebaeksan

Drumian

Shallow

subtidal

rplatform

Thrombo

lite-spon

gereefs

esmostlyAntha

spidellid

onstructed

andmicrobial

tweenmesoc

kenLimestone

rginaBa

Australia

erDrumian

last-richrampde

Angustic

ellularia-Ta

ninia-lithistid

ankenella

)reefe

certain

possibly

decimeters

gesmainlypa

ssivereef

erswithinmatrixform

Angustic

ellulariaan

andReitner

-Molla

Paibian

Subtidalp

latform

margin

Lithistidspon

ankenella

)-Girvanella

reefspo

volumean

eworkby

theirmutua

lattach

eworks

encrustedby

Girvanella

orministrom

atolite

95)Kruse

Zhurav

lev(200

nzaKingFo

rmation

dCalifornia

Paibian

lwithinshallow

subtidal

Lithistidspon

allatin

ospongia)-de

ndrolitereefs

closed

ndrolite

inarea

dRigby

Shallow

marine

Lithistidspon

ilbernicyathu

irvanella

-Tarthinia

meter-scale

Tarthinia

Epiphy

Renalcisspon

nstitute

ofreef

volume

Shallow

subtidal

spidellid

icrobial

esform

entAngustic

ellulariagrew

athspon

microstromatolites

filltheinterspa

tweenspon

gefram

eworks

sometim

curwithinspon

Mrozeket

Dotsero

Colorad

erStag

Shallow

marine

Girvanella

- Tarthinia-lithistidspon

ilbernicyathu

s)reefthinve

Girvanella

stromatolite

substantially (Zhuravlev et al 1993 Scrutton 1997) but both groupspersisted Two examples of archaeocyaths occur in the Drumian (Woodet al 1992 ~500ndash504Ma Bassett-Butt 2016) and late Cambrian(Furongian) (Debrenne et al 1984) of Antarctica but the group did notregain its former prominence or form reefs (Bambach et al 2002) andis not known in the Ordovician Midndashlate Cambrian conical cor-alomorphs include Cothonian and Lipopora in Age 4 and Tretocylichne inAge 5 (Park et al 2016 figs 4 5) and the similar genus Cam-broctoconus in late Age 5early Drumian (~504Ma) (Park et al 2011)which was a reef-building component (Lee et al 2016a) Cambrotrypa(Fritz and Howell 1959 Bolton and Copeland 1963 Scrutton 1979Jell 1984) from the middle Cambrian of North America could be arecumbent cerioid to phaceloid coral (Scrutton 1997) In contrast toarchaeocyaths coralomorphs (eg Amsassia) recovered in the EarlyOrdovician

35 EarlyndashMiddle Ordovician (485ndash460Ma) microbial-lithistid-calathiid-pulchrilaminid

Early Ordovician lithistid-microbial reefs broadly resemble thoseof the midndashlate Cambrian but the lithistids are larger (egArchaeoscyphia) (Fig 4) and an additional cuplike group the calathiidsappeared exemplified by Calathium from the late TremadocianearlyFloian (Church 1974) The major change at this time however was theappearance of a variety of encrusting-domical forms that includedpulchrilaminids coralomorphs (Amsassia) and the first definite ap-pearances of tabulate corals (Lichenaria) bryozoans (Nekhorosheviella)and stromatoporoids (Cystostroma) These encrusting skeletons pro-gressively transformed reef structure (Kroumlger et al 2017) Pulchrila-minids (Pulchrilamina Zondarella) can be up to 1m in size half as largeagain as early Cambrian Flindersipora These reefs locally formed ske-letal frameworks and hosted cryptic benthic organisms (Hong et al2014 2015 Li et al 2017b) (Fig 4) This significant increase in

skeletal reef-builders has been regarded as an initial phase of the GOBEforeshadowing the subsequent importance of reef-building stromato-poroids and tabulate corals (Webby 2002 Webby et al 2004 Adachiet al 2011)

351 Receptaculitids radiocyaths cyclocrinitidsThese calcified cup-like pear-shaped or globular macrofossils differ

in age and their affinities (generally suggested to be sponge or algal)continue to be debated Radiocyaths are restricted to the earlyCambrian (Kruse et al 2015) where they are generally minor reefcomponents They were initially compared with archaeocyaths(Bedford and Bedford 1934) with which they are associated in reefconstruction but they differ in structure (Debrenne et al 1970) Re-ceptaculitids appear ~478Ma (TremadocianFloian) and Calathium is acommon frame-builder in Early Ordovician reefs (Church 1974 2009Toomey and Nitecki 1979 Cantildeas and Carrera 1993 Li et al 20142015 Shen and Neuweiler 2018) Ordovician receptaculitids are di-verse and have been subdivided into three main groups ischaditidsreceptaculitids soanitids (or calathiids) (Nitecki et al 2004 fig 311)They are locally important in later Ordovician reefs (eg Kroumlger et al2014) and range to the late Paleozoic Cyclocrinitids mainly occur inthe midndashlate Ordovician and were diverse (eg Apidium Coelo-sphaeridium Cyclocrinites) near the SandbianndashKatian transition (Niteckiet al 2004)

Receptaculitids radiocyaths and cyclocrinitids have been comparedbecause their walls are composed of numerous small plates that create adistinctively patterned external surface and bear internal rods Thesestructural similarities are greatest between radiocyaths and re-ceptaculitids (Nitecki and Debrenne 1979) and more superficial incyclocrinitids (Beadle 1988) Cyclocrinitids have long been comparedwith dasycladalean algae (Stolley 1896) whereas receptaculitids(Austin 1845 Billings 1865) and radiocyaths (Bedford and Bedford1934) were both initially regarded as sponges This long-established

Sponge width (cm)

Reef width (m)0 1 10 100

skeletal component

microbial component

0 5 10 15

Zhangxia Fm Ranken Lm Deh-Molla Fm Notch Peak Fm

~521 ~509 ~497 485

~529 470 Ma

Tremadocian Floian

Early Ordovician

Drumian Pai-bian

Jiang-shanian

Fig 4 Summary of Cambrian and Early Ordovician reefs (A) Size of reef-building sponges (B) Size of reefs in log-scale (C) Pie diagrams of main reef-buildingcomponents (microbial vs skeletal) See Table 1 for data sources

distinction was challenged by the proposal that the receptaculitidIschadites is - like cyclocrinitids - a dasycladalean alga (Kesling andGraham 1962 Byrnes 1968) Support for this view not only resulted init being applied to receptaculitids in general but also in cyclocrinitidsbeing regarded as receptaculitids (Nitecki 1970 1972 Nitecki andDebrenne 1979 Rietschel and Nitecki 1984)

Such sweeping interpretations attracted some opposition Rietschel(1977) agreed that receptaculitids are algae but considered that theyare not dasycladaleans Beadle (1988) argued that receptaculitids anddasycladaleans are lsquoentirely unrelatedrsquo These discussions were oftencomplicated by being a part of the parallel debate about archaeocyathaffinities (Rowland 2001) Nitecki et al (1999 2004) suggested thatcyclocrinitids are algae similar to dasyclads but that receptaculitids areneither algae nor sponges This latter view was also often considered forarchaeocyaths (Vologdin and Zhuravleva 1947 Zhuravleva andMyagkova 1987) before they became generally regarded as sponges(Debrenne et al 2015b)

One of the difficulties in determining receptaculitid affinities is themorphological heterogeneity of the group ranging from enclosedpyriform to bowl-shaped bodies (Byrnes 1968) Calathiids includingCalathiumSoanites are clearly conical or cup-like (Myagkova 1966Church 1991) This morphology common in filter-feeding organisms(Billings 1865 Myagkova 1966 Li et al 2015 2017b) supportsBillings (1865) early view that Calathium is a sponge A parsimoniousview might be that radiocyaths (and cuplike receptaculitids ie ca-lathiids) are sponges and that cyclocrinitids (perhaps together withenclosed receptaculitids) are algae If radiocyaths and receptaculitidsare related then radiocyath decline at the end of the early Cambrianfollowed by the Early Ordovician appearance of the calathiids could bea further example of a group that was reduced in diversity and abun-dance during the midndashlate Cambrian but recovered in the Early Ordo-vician More information is required to elucidate these possibilities

352 BryozoansThe early history of bryozoans is problematic The affinity of

Dresbachian (Fritz 1948) (~499Ma) Archaeotrypa (Fritz 1947) is un-certain it may be a bryozoan or echinoderm (see Scrutton 1979 Jell1984 Kobluk 1984 Rozanov and Zhuravlev 1992 Zhuravlev et al1993) Pywackia reported by Landing et al (2010) from CambrianStage 10 of Mexico has been compared with octocorals (Taylor et al2013 but see Landing et al 2015) The earliest currently unquestionedbryozoan is Prophyllodictya from lower Tremadocian wackestones ofSouth China (Ma et al 2015) and the earliest reef-building bryozoan islate Tremadocian (~479Ma) laminar Nekhorosheviella semisphaericaalso from South China (Cuffey and Zhu 2010 Adachi et al 2012Cuffey et al 2013 fig 24a) Nekhorosheviella mutually encrusts canoccur on lithistids and together with crinoid holdfasts forms smallmounds 30 cm wide and 10 cm high similar to Middle Ordovicianpelmatozoan patch reefs (Pratt 1989 Adachi et al 2011) Largerbryozoan reefs appear in the late Darriwilian (Pitcher 1964)

353 PulchrilaminidsLate Tremadocian (~480Ma) Pulchrilamina (Toomey and Ham

1967) and Dapingian Zondarella (Keller and Fluumlgel 1996) are by far thelargest Early Ordovician skeletons although they often enclose or areinterlayered with sediment Pulchrilaminids share similarities withstromatoporoids but their characteristic features such as very thin la-tilaminae and lsquomore loosely aggregated meshwork of skeletal elementsincluding slender upwardly tapering spinose rods that are spiculelikersquosuggest they are an independent group (Webby 2015)

354 CoralsLichenaria generally considered the earliest tabulate coral

(Scrutton 1997 Elias et al 2008) is recorded from the early Trema-docian (Pratt and James 1982) (their Green Head Mound occurs in thelower Tremadocian Watts Bight Formation See Knight et al 2008 p

118) However Laub (1984) regarded the earliest Lichenaria as Darri-wilian and therefore contemporaneous with other tabulates such asBillingsaria and Eofletcheria (Desrochers and James 1989 Pickett andPercival 2001 Kroumlger et al 2017) The coralomorph Amsassia (Carreraet al 2017) may have been confused with Lichenaria but differs ingrowth mode and has been suggested to be an alga (Sun et al 2014)

36 Late MiddlendashLate Ordovician (460ndash444Ma) stromatoporoid-bryozoan-tabulate-receptaculitid-microbial

Stromatoporoids appear in the Early Ordovician (early Floian) assmall specimens of the labechiid Cystostroma attached to Calathium (Liet al 2017b) Much larger labechiids (Labechia Pachystylostroma) andalso clathrodictyiids (Pseudostylodictyon) appear in the late Darriwilian~460Ma (Pitcher 1964) Together with bryozoans (Batostoma) andtabulate corals (Billingsaria) as well as the chaetetid Solenopora theyconstructed large DarriwilianSandbian reefs such as the classic Chazyexamples in Vermont (Pitcher 1964 Finks and Toomey 1969 Kapp1975) and the upper Sandbian Carters Formation of Tennessee(Alberstadt et al 1974) In addition to their size and abundance mid-Ordovician stromatoporoids bryozoans and tabulates are also notablefor their laminar and domical shapes (Copper 1974 Fagerstrom 1987Webby 2002 Webby et al 2004 Adachi et al 2011) which trans-formed substrate colonization and vertical succession in reefs (Pitcher1964 Finks and Toomey 1969 Alberstadt et al 1974 Copper 1974Hong et al 2017 2018 Kroumlger et al 2017) Rugose corals also appearin the late Darriwilian but did not become common until the Sand-bianndashKatian (Baars et al 2012) All these groups diversified further inthe Late Ordovician together with encrusting echinoderms cuplikereceptaculitids and globular cyclocrinitids Skeletal reefs with bivalvessiliceous sponges and the coralomorph Amsassia also occur during thistime interval (Lee et al 2014c 2016b Sun et al 2014) These de-velopments were part of continued GOBE diversification in the Middleto Late Ordovician that resulted in complex and well-structured benthiccommunities (Droser and Sheehan 1997 Webby 2002 Harper 2006)Lithistids often in association with Calathium and microbial carbonatescontinued to be locally abundant in late Darriwilian reefs (Alberstadtet al 1974 Klappa and James 1980 Desrochers and James 1989Brunton and Dixon 1994 Liu et al 2003 Li et al 2017c) but thevolumetric importance of these components appears to have declinedby the Late Ordovician as stromatoporoids corals and bryozoans in-creased (Webby 2002 Adachi et al 2011)

4 Midndashlate Cambrian lithistid sponge-microbial reefs

The nature and distribution of lithistid sponge-microbial reefs arecentral to our discussion of midndashlate Cambrian environments andbiotas Following their discovery in lower Furongian strata of Iran(Hamdi et al 1995) midndashlate Cambrian LSM reefs have been re-cognized worldwide (Mrozek et al 2003 Shapiro and Rigby 2004Johns et al 2007 Kruse and Zhuravlev 2008 Hong et al 2012 2016Kruse and Reitner 2014 Adachi et al 2015 Lee et al 2016a)(Table 1) In contrast to early Cambrian archaeocyath-microbial reefsand Early Ordovician lithistid sponge-microbial reefs which have beenstudied in detail for more than 100 years middlendashlate Cambrian LSMreefs remain much less well-known Here we briefly summarize thecomposition and structure of four relatively well-described examples

41 Zhangxia Formation (upper Stage 5 Cambrian Series 3) ShandongChina

The oldest LSM reefs currently known occur in the lower part of theZhangxia Formation (Shandong Province China) (Woo 2009 Adachiet al 2015) where they form lenses ~150 cm thick within microbialmounds (Lee et al 2016a) Based on the trilobite biozone Lioparia theybelong to the upper part of Stage 5 of Cambrian Series 3 At this level

the Zhangxia Formation is mainly composed of bioturbated wackestoneand oolitic skeletal and peloidal packstone-grainstone deposited on ashallow subtidal carbonate platform (Woo 2009 Lee et al 2015b)Metazoans include the lithistid sponge Rankenella zhangxianensisLeeet al 2016d (Family Anthaspidellidae Order Orchocladina) the stem-group cnidarian Cambroctoconus orientalisPark et al 2011 and uni-dentified siliceous sponges (Fig 5A) Microbial components includeEpiphyton microstromatolite and undifferentiated microbialite (Leeet al 2016a) (Fig 6A B) R zhangxianensis occupies up to 20 of thereef volume is mostly conical in shape with smooth outlines and is3ndash21mm in diameter and up to 610mm in length C orientalis(8ndash11mm in diameter 11ndash13mm in length Park et al 2011) is shapedlike an octagonal cone and occupieslt 3 of the reef volume Theunidentified siliceous sponges (~1 of reef volume) consist of irregu-larly shaped spicule networks resembling keratose sponges (cf Luo andReitner 2014) Small dendritic calcified epiphytaceans are a majorcomponent up to 20 of the reef volume Microstromatolites arecharacterized by thin convex-up laminae of alternating dark and lightgray micrite Undifferentiated microbialite composed of clotted-pe-loidal fabric with faint laminae possibly represents poorly preservedmicrostromatolite The main framework builders are the lithistidsEpiphyton and stem-group cnidarians (Lee et al 2016a) The lithistidsand stem-group cnidarians locally mutually attach (Fig 5A) whereasEpiphyton is either mutually attached or attached to the sponges Thesemetazoan-calcimicrobial frameworks were encrusted and stabilized bymicrostromatolite (Fig 6A B) and probably created at least a fewcentimeters of synsedimentary relief

42 Ranken Limestone (upper Drumian Cambrian Series 3) GeorginaBasin Australia

Reef fabrics formed by lithistid sponges and microbes in the RankenLimestone are only known from loose blocks described by Kruse andReitner (2014) who supposed that the individual reefs would not haveexceeded a few decimeters in size The Ranken Limestone consists ofcross-bedded bioclast-ooid-intraclast grainstone and subordinate bio-clastic wackestone and appears to be a ramp deposit Biostratigraphiccontrol is poor but relationships with adjacent deposits suggest a lateDrumian age (Kruse and Reitner 2014) The reef fabric mainly consistsof microstromatolite and the anthaspidellid sponge RankenellamorsKruse 1983 (Kruse and Reitner 2014) (Fig 5B) which is mostlyexplanate in shape and only about 1mm thick although conical ex-amples are also present Domical or locally columnar masses of mi-crostromatolite up to 11mm thick and 26mm across consist of lightand dark laminae with patches of calcified microbes (AngusticellulariaTaninia) The Ranken reef is therefore mainly microbial and the role ofR mors appears to have been subordinate mainly providing a substratefor stromatolite growth Elsewhere in the Georgina Basin R mors in-habited low-energy anaerobic mudstone environments in the mid-Cambrian Arthur Creek Formation (Kruse 1996 Debrenne and Reitner2001)

43 Deh-Molla Formation (lower Paibian Furongian) northern Iran

These generally small LSM reefs less than a few tens of centimeters

Fig 5 Examples of midndashlate Cambrian reef-building sponges (A) Rankenella zhangxianensis (upper Stage 5 Zhangxia Formation) Beiquanzi section ShandongProvince China (B) R mors (upper Drumian Ranken Limestone) locality NTGS4648 Georgina Basin Australia (after Kruse and Reitner 2014 fig 5A) (C) R hamdii(lower Paibian Deh-Molla Formation) Shahmirzad section northern Iran (after Kruse and Zhuravlev 2008 fig 7D) (D) Unidentified anthaspidellid sponge (Stage10 Notch Peak Formation) Arrow Canyon section Nevada USA Coin is 19mm in diameter

in height and width (Hamdi et al 1995 Kruse and Zhuravlev 2008)occur in the Mila (renamed Deh-Molla) Formation (Geyer et al 2014)The reef-bearing interval overlies the Prochuangia trilobite biozonesuggesting an early Furongian (Paibian) age (Peng et al 1999) Theplatform margin on which it developed preserves microbial bound-stonefloatstone with abundant demosponges (Geyer et al 2014) Themain reef components are Rankenella hamdii (anthaspidellid sponge)and Girvanella (calcified cyanobacterium) R hamdii occupies up to50 of the reef volume (Hamdi et al 1995) It is conical bowl ordigitate in shape (Fig 5C) 4ndash31mm in diameter and up to 80mm inheight and mutually attaches forming frameworks that are commonlythickly encrusted by Girvanella columnar microstromatolites andclotted-peloidal fabric These encrustations mainly occur on the dermalsurfaces of the sponges but sometimes also on the gastral surfaces(Fig 5C)

44 Notch Peak Formation (Stage 10 Furongian) Nevada USA

Anthaspidellid sponge-microbialite reefs occur in the upper part ofNotch Peak Formation (Mrozek et al 2003) Oolitic and bioclasticpackstone-grainstone and flat-pebble conglomerates as well as stro-matolites and the lithistid sponge-microbial reefs are locally well-pre-served within an otherwise dolomitized succession The facies asso-ciation suggests a shallow subtidal environment The reefs are domicaland a few meters thick commonly occurring with columnar stroma-tolites (Mrozek et al 2003) They contain the Eoconodontus notchpea-kensis conodont fauna suggesting a late Furongian (Age 10) age(Mrozek et al 2003 Dattilo et al 2004) Three main components of

these LSM reef are unidentified lithistid sponge microstromatolite andthe calcified microbe Angusticellularia (Mrozek et al 2003 J-HLpersonal observation) (Figs 5D and 6C D) The lithistids are mainlythin walled (~5mm) upward widening cups (often 3 cm but up to14 cm in diameter) They do not appear to closely resemble any de-scribed lithistid genus but display typical anthaspidellid-type spiculenetworks (J-HL personal observation) The microstromatolites consistof thin alternating light-dark laminae grading to faintly clottedlami-nated fabric Dark pendent Angusticellularia is common on the lowersurfaces of the sponges Keratose-like siliceous sponges occur rarelywithin the lithistid spongocoels The main frame-builders of theseNotch Peak reefs are lithistids which appear to have been firmly mu-tually attached The downward growing Angusticellularia althoughforming only very thin crusts suggests sediment-free space beneath thegrowing sponges Bioturbated micrite skeletal fragments and uni-dentified siliceous sponges fill the spongocoels Microstromatolites oc-cupy much of the space between sponges (Fig 6C) and thin micro-stromatolite layers locally encrust sponge dermal surfaces withinspongocoels (Fig 6D)

45 Summary

Although much further research is required in structure and com-position these midndashlate Cambrian LSM reefs quite closely resembleEarly Ordovician examples built by microbes and the lithistidArchaeoscyphia The above examples suggest several general char-acteristics of late Cambrian LSM reefs 1 Decimeter- to meter-scalelensoid to domal shape 2 Co-occurrence with and often within

Fig 6 Photomicrographs of lithistid sponges and microstromatolites in midndashlate Cambrian reefs (A B) Rankenella zhangxianensis-Epiphyton-Cambroctoconus orientalisreef (upper Stage 5 Zhangxia Formation) Beiquanzi section Shandong Province China (C D) Anthaspidellid sponge-microbial reef (Stage 10 Notch PeakFormation) Arrow Canyon section Nevada USA

microbial reefs 3 Mutually attached frameworks formed by sponges 4Microstromatolites encrusting and stabilizing the sponge frameworks5 Formation in shallow subtidal packstone-grainstone environments

5 Midndashlate Cambrian dysoxia-hypoxia and sponge-microbial reefs

51 Evidence for low-oxygen conditions

A minimum level of oxygen required to maintain aerobic metabo-lism has long been linked to animal diversification during theProterozoicndashCambrian transition (Berkner and Marshall 1965 Rhoadsand Morse 1971 Knoll and Carroll 1999 Canfield et al 2007 Payneet al 2009 2011 Dahl et al 2010 Maloof et al 2010a Knoll 2011Sperling et al 2013 Ader et al 2014 Mills and Canfield 2014 Xiao2014 Zhang et al 2014 2018 Chen et al 2015 Li et al 2017aShields 2017) It has been suggested that ocean oxygenation promotedanimal diversification in the early Ediacaran ~630Ma (Sahoo et al2012) and earlyndashmid (541ndash509Ma) Cambrian (Li et al 2017a) andthat lsquomodern-like oxygen levelsrsquo appeared by ~521Myr ago (Chenet al 2015) However evidence from iron speciation (Sperling et al2015a) Mo-isotopes (Dahl et al 2010) and alteration of deep sea ba-salts (Stolper and Keller 2018) provide compelling evidence that per-sistent elevated oxygen levels are likely a later Paleozoic phenomenonIt seems that oxygenation of the oceans during the Ediacaran-Cambriantransition was likely a protracted and fluctuating series of oxic-anoxiceuxinic phases (Fike et al 2006 Canfield et al 2007 2008 Shen et al2008 Jiang et al 2009 Halverson et al 2010 Wood et al 2015Zhang et al 2018 Wood and Erwin 2018) This secular pattern wasfurther complicated by local variations in basinal and shelf anoxia(Goldberg et al 2005 Schroumlder and Grotzinger 2007 Canfield et al2008 Kendall et al 2015 Sperling et al 2015a Jin et al 2016 Ochet al 2016 Cheng et al 2017) Moreover the tendency toward lowseawater oxygen concentrations subsequently appears to have in-creased during the Cambrian (Boyle et al 2014 Cremonese et al2014) and persisted into the Ordovician (Railsback et al 1990Strauss 2006 Kah and Bartley 2011 Thompson and Kah 2012Wallace et al 2017) (Fig 1) Based on extensive black shale occur-rences Berry and Wilde (1978) inferred widespread and recurrentepisodes of marine hypoxia during the midndashlate Cambrian and EarlyOrdovician They compared these conditions with those of the Cretac-eous attributed them to elevated temperatures and suggested that theydid not decline until cooling promoted mid-Ordovician ocean ventila-tion (Fig 1) Black (or dark-colored) shales have been widely re-cognized in lower Paleozoic strata worldwide (eg Leggett 1980Wilde and Berry 1984 Berry et al 1986 1989 Wilde et al 1989Fyffe and Pickerill 1993 Saltzman et al 2000 Egenhoff et al 2015)The Chengjiang (ca 520Ma) Burgess Shale (ca 508Ma) and Fezouata(ca 480Ma) biotas as well as other Burgess-Shale type biotas whichrecord a large proportion of early animal taxa are preserved in organic-rich shales that are thought to reflect low-oxygen conditions (ConwayMorris 1986 Gaines et al 2005 Gaines and Droser 2010 Van Royet al 2010) even though other factors could have been necessary topreserve these fossils (Gaines 2014) Some of these shales are sig-nificant sources of petroleum (eg Buchardt and Lewan 1990 Miet al 2007 Ryder et al 2014) and gas (eg Yu et al 2009 Schovsboet al 2011 Huang et al 2012 Pashin et al 2012 Pool et al 2012)Preservation of abundant organic matter in these shales suggests thatlow-oxygen conditions were prevalent throughout their depositionExtinctions of archaeocyaths (Zhuravlev and Wood 1996) and trilo-bites (Palmer 1984 Westrop and Ludvigsen 1987) in the Cambrianhave been linked to anoxia

This broad interpretation of a tendency to low oxygen marineconditions during the interval between the early Cambrian and mid-Ordovician has received support from studies of biogeochemically cy-cled redox-sensitive elements (C N S U isotopic values and ZnFeMo CeCe ThU abundances) particularly for the midndashlate Cambrian

(Perfetta et al 1999 Saltzman et al 2000 Gill et al 2011 Dahl et al2014 Saltzman et al 2015) Well documented examples of corre-spondence between black shale deposition faunal change and geo-chemical indicators of hypoxia include the ~510Ma Sinsk and~500Ma SPICE events Incursions of anoxic water onto shelves at~510Ma have been inferred from negative carbon isotope (Montantildeezet al 2000 Guo et al 2010) and positive δ34S (Hough et al 2006)values Similar age δ15N values among the lowest of the Phanerozoicmay suggest low-oxygen photic zone conditions (Algeo et al 2014 fig1) Interpretation of the ~500Ma Steptoean Positive Carbon IsotopeExcursion (SPICE) as reflecting low-oxygen conditions in shelf waters(Saltzman et al 2000) is supported by coeval positive δ34S sulfateexcursions (Gill et al 2007 2011 Hurtgen et al 2009) decreased Moenrichment (Gill et al 2011) and negative δ238U excursion (Dahl et al2014) In addition the Drumian (middle Cambrian) negative carbonisotope excursion (DICE) (~505Ma) and associated Mo U and V va-lues have been linked to euxinic conditions that extended into thephotic zone (Pagegraves and Schmid 2016) CambrianndashOrdovician boundary(~485Ma) slope carbonates in Newfoundland have CeCe and ThUratios and N and U-isotope values consistent with dysoxic conditions(Azmy et al 2014 2015) The inference of Berry and Wilde (1978)that the tendency for shelf biotas to experience influxes of low-oxygenwaters only diminished in the mid-Ordovician as ocean circulationimproved is supported by oxygen (Railsback et al 1990) and sulfur(Kah et al 2016) isotope studies as well as ThU ratios in carbonates(Marenco et al 2016) and has been linked to global cooling (Trotteret al 2008) (Fig 1)

These changes are widely considered to have been important inushering in the GOBE (McKenzie et al 2014 Saltzman et al 2015)Edwards et al (2017) suggest that atmospheric oxygen concentrationswere low (~12) during the Early Ordovician and doubled to about25 by the Darriwilian coinciding with increased biodiversity Basedon sea-surface temperature (Trotter et al 2008 fig 3) and modeledestimates of atmospheric oxygen (Edwards et al 2017 fig 2) wecalculated the dissolved oxygen concentrations in seawater during theOrdovician (Fig 7) These values are generally near 100 μM during theEarly Ordovician approximately one third of present-day seawaterThey begin to rise ~465Ma (early Darriwilian) and reach a peak at451Ma (early Katian) before declining steeply to 446Ma (late Katian)This overall trend broadly corresponds with that of marine invertebratediversity (Sepkoski Jr 1995 fig 1 Webby et al 2004 fig 11) Ourcalculated dissolved oxygen values (Fig 7) from Edwards et al (2017fig 2) are mainly for the Ordovician but also indicate ~12 atmo-spheric oxygen in the late Cambrian Based on the minimum require-ments of animals (lower value) and pervasive subsurface anoxia (uppervalue) Sperling et al (2015b fig 3) (also Stolper and Keller 2018)estimated overall Cambrian atmospheric oxygen levels to have beeneven lower in the range 15ndash40 of present atmospheric level (= 3ndash8oxygen) These average values can be expected to have resulted inmuch lower levels of dissolved oxygen seasonally and locally Even inthe present-day ocean under 21 atmospheric O2 hypoxia commonlydevelops (Rabalais et al 2010) and oxygen-deficient waters threatencoral reefs (Altieri et al 2017) There is evidence for early to middleCambrian oxygen-minimum zones (Guilbaud et al 2018) It is there-fore likely that localized and seasonal conditions resulted in fluctua-tions well below the average level of dissolved oxygen (~100ndash115 μML) that we calculated (Fig 7) for the Early Ordovician and which isalready hypoxic according to the definition of Tyson and Pearson(1991)

Terms commonly used to describe dissolved oxygen levels includeanoxic suboxic dysoxichypoxic oxicnormoxic (eg Tyson andPearson 1991 Middleburg and Levin 2009 Rabalais et al 2010Sperling et al 2015a) These terms the thresholds defining them andthe units used to measure them (eg mgL μMkg mLL μML) oftendiffer according to author and research field Tyson and Pearson (1991table 2) pointed out that terms such as dysoxic dysaerobic and hypoxic

had been applied to environment biofacies and physiology respec-tively Over time however some of these distinctions have becomeblurred The following terms (for environments facies oxygenationlevels) and thresholds were recommended by Tyson and Pearson (1991table 2) in mLL at 10 degC 1 atm pressure with 1029 density of sea-water (conversions to other widely used units are shown in brackets)

oxic 80ndash20 mLL (= 1203ndash301mgL 376ndash94 μML3654ndash9135 μMkg 1169ndash292 ppm)

dysoxic 20ndash02 mLL (= 301ndash030mgL 94ndash94 μML9135ndash914 μMkg 292ndash029 ppm)

suboxic 02ndash00 mLL (= 030ndash0mgL 94ndash0 μML 914ndash0 μMkg029ndash0 ppm)

anoxic ge00 mLL (= ge0 in all cases)Unlike reef-builders mobile organisms can move to avoid localized

environmental changes Furongian and Early Ordovician reefs inNewfoundland for example occur in close association with skeletons oftrilobites and cephalopods (see Pruss and Knoll 2017) Several present-day groups including shrimps and crabs can detect and avoid oxygendeficient sea water (Renaud 1986) Mobile nekton on the northern Gulfof Mexico continental shelf avoids oxygen levelslt 2mgL (14 mLL)(Pavela et al 1983 Renaud 1986) and fish avoidance generally oc-curs at oxygen concentrations 05 to 2mgL (035 to 14 mLL) (Levinet al 2009) Similarly various motile organisms including cteno-phores crustaceans and cephalopods can tolerate low oxygen levels(Ekau et al 2010 table 2) Variability in oxygen concentrations can bemore limiting than the absolute value (Matabos et al 2012) There isevidence that late Cambrian groups such as olenids (Fortey 2000) and

phosphatocopids (Williams et al 2011) were dysoxia-tolerant Largepresent-day arthropods such as lobsters are relatively tolerant ofoxygen levels as low as 2 ppm though 4 ppm is generally considered tobe the minimum (Bayer et al 1998) Our calculation of ~100 μMoxygen (32 ppm) in the Early Ordovician is approaching the upperlimit of dysoxic (292 ppm) based on Tyson and Pearson (1991 table 2)This suggests that average oxygen levels in Early Ordovician seawatercould have supported large arthropods but that seasonal and localvariations could readily have resulted in oxygen limitation

52 Factors promoting low-oxygen conditions in shallow marineenvironments

Interrelated factors generally contributing to shallow marine deox-ygenation include global warming increased marine productivitythermal stratification and expansion of shallow platform areas(Schmittner et al 2008 Keeling et al 2010 Praetorius et al 2015)Global warmth that characterized the mid-Cambrian to mid-Ordovi-cian (Frakes et al 1992 p 14) and promoted low-oxygen conditionshas been linked to high sea-level and high CO2 ldquogreenhouserdquo conditionsduring commencement of the first Phanerozoic supercycle (Fischer1984 Landing 2012b Nance and Murphy 2013) Modeled estimatessuggest that CO2 (Berner 2009) and temperature (Royer et al 2004fig 4) peaked in the mid-Cambrian Oxygen isotope thermometry in-dicates earliest Ordovician sea-surface temperatures (Shields et al2003 Kasting et al 2006) in excess of 40 degC (Trotter et al 2008)Earlier additional episodic warming due to CO2 increase has been

n micro

Early Ordovician470 4584

Middle Ordovician Late Ordovician4438 Ma

LateCamb

Fig 7 (A) Ordovician marine invertebrate diversity (Sepkoski Jr 1995 fig 1) (B) Dissolved oxygen concentrations in seawater calculated from sea-surfacetemperature (Trotter et al 2008 fig 3) and atmospheric oxygen (Edwards et al 2017 fig 2) data (see Supplementary Oxygen and Temperature Data)

attributed to extensive continental flood basalt volcanism such as thelate Cambrian Age 4 Kalkarindji Large Igneous Province in Australia(5107 plusmn 06Ma Jourdan et al 2014) (Glass and Phillips 2006Hough et al 2006) As shown by Mesozoic Ocean Anoxic Events(OAEs) clear links can exist between anoxia and Large Igneous Pro-vinces (LIPs) However further studies are needed to identify PaleozoicLIPs (Percival et al 2015 fig 1) and disparities in timing betweenearly Botomian anoxia (gt 514Ma Peng et al 2012) the Hawkes Bayregression (~511Ma) and the Kalkarindji eruption (~510Ma) re-commend caution in linking these events

Low oxygen areas develop or persist seasonally or continuouslybeneath upwelling regions associated with the upper parts of oxygenminimum zones and in warm oceans that are more stratified hold lessoxygen and experience greater advection of oxygen-poor source waters(Levin et al 2009) In addition to lowering oxygen solubility highertemperatures make water less dense promoting thermal stratificationthat in turn reduces ventilation (Erbacher et al 2001) Warming alsofavors biological productivity in the water column (eg phytoplanktonblooms) which increases carbon burial and thus the likelihood ofbottom-water hypoxia (Pedersen and Calvert 1990 Sen Gupta et al1996) Global Cambrian sea-level rise (Miller et al 2005) promoteddevelopment of extensive shallow epeiric carbonate platforms (Petersand Gaines 2012) that tend to limit shallow-water circulation (Irwin1965) and expand the environments subject to thermal stratification(Allison and Wright 2005 Allison and Wells 2006) In Laurentia mid-Cambrian sea-level rise established extensive platforms that locallypersisted into the Late Ordovician (Bond et al 1989 Morgan 2012)This lsquoGreat American Carbonate Bankrsquo enclosed intrashelf basins (egMarkello and Read 1981) prone to dysoxia-anoxia and black mud-stones accumulated on its slopes during eustatic highs (Landing 2012a2012b Lavoie et al 2012 Miller et al 2012 Peters and Gaines 2012)These conditions ameliorated by the mid-Ordovician as indicated byearly Darriwilian sulfur isotope values consistent with ocean ventilationthat appear to coincide with lower sea-surface temperatures (Kah et al2016) as well as with decrease in strontium isotope values (Edwardset al 2015) Ordovician cooling and oxygenation coincident with di-versification of the ldquoPaleozoicrdquo and ldquoModernrdquo faunas (Trotter et al2008) also marked the end of sponge-microbial reef dominance in theearly Paleozoic (Brunton and Dixon 1994) This trend continued untilwidespread oxygenation of the deep ocean occurred in the mid-Paleo-zoic (Dahl et al 2010)

53 Low oxygen levels and lithistid sponges

Lithistids are a polyphyletic group of demosponges with interlockedsiliceous spicules (desmas) that form a rigid skeleton (Hinde 1883Leacutevi 1991 Debrenne and Reitner 2001 Pisera 2002 Pisera and Leacutevi2002 Hill et al 2013) They are represented by about 46 extant genera(Maldonado et al 2016) Present-day lithistids can dominate benthicfaunas at depths of ~150ndash1800m (Kelly 2007) and locally aggregateinto reefs (Conway et al 1991) similar to ancient examples (Bruntonand Dixon 1994) Dense intertwined clusters of the lithistid Leio-dermatium pfeifferae with thin (3ndash9mm) erect foliose branches up to~80 cm high and 1m wide at depths of ~750m in the western Med-iterranean have been compared with Mesozoic lithistid reefs(Maldonado et al 2015 2016) However since the anthaspidellid li-thistids that dominated CambrianndashOrdovician reefs went extinct in thePermian caution is required when comparing lithistid reefs of differentages (Pisera 2002)

Data concerning the oxygen requirements of present-day lithistidsare limited more information is available concerning other demos-ponges and also hexactinellids Many sponges survive periods of anoxiaIn experiments demosponges not only tolerate hypoxia but appear tohave higher survival rates under hypoxic conditions than under nor-moxia (Gunda and Janapala 2009) Halichondria panicea for examplegrows under oxygen in the range 05ndash4 of present atmospheric level

(Mills et al 2014) Similar examples are documented from the wildFor example in Saanich Inlet western Canada hexactinellids surviveanoxia (oxygen concentrationslt 02mLL) (Tunnicliffe 1981) readilytolerate hypoxia (lt 14 mLL) (Chu and Tunnicliffe 2015) and gen-erally appear to do well in oxygen as low as 05mLL (ie severe hy-poxia) (Jackson Chu pers comm 2016) Thus overall at least somesponges dominate hypoxic systems and tolerate periodic anoxia(Hoffmann and Schlaumlppy 2011 Steckbauer et al 2011 Riedel et al2014)

Sponge cells together with their associated symbiotic microbes oftenexperience anaerobic conditions when pumping activity stops and canmaintain internal suboxic and locally hypoxic conditions (Hoffmannand Schlaumlppy 2011 Lavy et al 2016) Sponges typically use only asmall fraction of available oxygen for respiration (Hoffmann et al2005) and their ability to tolerate low oxygen levels may be linked tofacultatively anaerobic mitochondria (Mentel et al 2014) Somesponges including lithistids (Bruumlck et al 2012) harbor large numbersof bacterial symbionts (Imhoff and Truumlper 1976 Fan et al 2012) thatcan constitute up to 40 of sponge biomass (Taylor et al 2007Schmitt et al 2012) and provide significant nutrition These includeanaerobic bacteria that occupy ldquoanoxic nichesrdquo (Schlaumlppy et al 2010)The complex lithistid microbiome (Hentschel et al 2012) is a source ofpharmaceutical metabolites (Thomas et al 2010)

Molds of sponges (Gehling and Rigby 1996) and phosphatizedsponges (Li et al 1998 Yin et al 2015) occur in the Ediacaran Spi-cules that have been reported (Brasier et al 1997) may have beenmisidentified (Antcliffe et al 2014 Muscente et al 2015) Biomarkers(Love et al 2009 Sperling et al 2010) suggest that demosponges andweakly calcified sponge-grade metazoans (Maloof et al 2010b) ap-peared even earlier (Erwin et al 2011) consistent with sponges havinglow oxygen requirements (Mills and Canfield 2014) Oxygen increaseduring the EdiacaranndashCambrian transition (Fike et al 2006 Chenet al 2015) does not appear to have been sustained (see Section 51)The appearance of archaeocyaths in the early Cambrian and their re-latively abrupt decline coincident with the anoxic Sinsk Event(Zhuravlev and Wood 1996) suggests that they may have been lesstolerant than lithistids to low oxygen conditions In contrast lithistidsappear unaffected by midndashlate Cambrian and Early Ordovician extinc-tion events attributed to anoxia (Saltzman et al 2015) The only gra-dual increase observed in sponge size through the mid-Cambrian toearly Ordovician (Fig 3) could reflect the need to maintain the ad-vantage of small body size under low-oxygen conditions (Payne et al2011)

Stromatoporoids and corals were important reef-builders from themid-Ordovician to Late Devonian (Fagerstrom 1987 Wood 1999James and Wood 2010) The lithistid-microbial association reappearedsporadically eg in the Late Ordovician (Brunton and Dixon 1994Leinfelder et al 2002 p 185) Late Silurian (de Freitas et al 1999)and in Early Carboniferous reefs (eg Mundy 1994 Webb 1999)following Late Devonian stromatoporoid extinction Similarly a varietyof sponges together with microbes occurs in reefs following the end-Permian extinction (Brayard et al 2011) Probably the most con-spicuous Mesozoic development of lithistid-microbial reefs was in themidndashlate Jurassic together with hexactinellid sponges (Leinfelder et al2002) Lithistid-microbial reefs are common in poorly oxygenated en-vironments in the Upper Jurassic of Germany and Middle to UpperJurassic of Spain and Portugal (Leinfelder et al 1994 1996) at depthsof 30ndash90m coeval with shallower water coral-sponge-microbial reefs(Leinfelder 2001 fig 18) This was a period of relatively warm con-ditions (Jenkyns et al 2012) when reduced oceanic circulation is in-ferred to have promoted black shale formations and dysaerobic reefs(Leinfelder et al 1994 1996) Lithistid-microbial reefs could thereforerepresent a default ldquolow oxygenrdquo Phanerozoic reef community

Stromatoporoids may have had different oxygen requirements fromlithistids Present-day hypercalcified sponges (sclerosponges) con-sidered to be relict stromatoporoids (Stearn 2015b) preferentially

occur in shallow water (~20m) with corals (Reitner 1993 Quinn andKojis 1999) Together with light dependence in Paleozoic stromato-poroids (Kershaw 2015 Stearn 2015a) and the depth-dependent oc-currence of hypercalcified sponges in Jurassic reefs (eg their dom-inance in shallow marine reefs and absence in deep poorly oxygenatedJurassic lithistid-microbial reefs) (Fuumlrsich and Werner 1991 Werneret al 1994) it can be postulated that stromatoporoids preferredshallow oxygen-rich environments

54 Mid-Cambrian to Early Ordovician reef development

It is now apparent that the midndashlate Cambrian ldquoreef gaprdquo was oc-cupied by LSM reefs and that early Cambrian archaeocyath-microbialreefs and Early Ordovician LSM reefs were broadly similar in structureto those of the midndashlate Cambrian Cambrian to Early Ordovician reefdevelopment prompts a number of key questions why did archae-ocyaths decline why were lithistids the only significant metazoan reefbuilders during the midndashlate Cambrian what factors could have limitedother reef builders during this period and what prompted the rise ofnew skeletal reef-builders in the Early Ordovician

Archaeocyath decline has been linked to one or more of sea-levelfall (Palmer and James 1979) anoxia (Zhuravlev and Wood 1996Zhuravlev 2001b) and ocean acidification (Knoll and Fischer 2011)all of which have also tentatively been related to the Kalkarindji floodbasalt eruptions (Glass and Phillips 2006 Hough et al 2006) Thesubsequent midndashlate Cambrian interval with reefs largely dominatedby calcimicrobes and microbial carbonates has been regarded as a post-extinction phase following archaeocyath demise in which microbesrepresent a ldquodisaster florardquo (Fagerstrom 1987 Zhuravlev 1996 Wood1999) Although it has been speculated that the microbes may haveoutcompeted metazoan reef-builders during this interval (Riding andZhuravlev 1994 Zhuravlev 1996 Rowland and Shapiro 2002) thisalone would not account for its ~25Myr duration which far exceedsrecovery from much larger subsequent extinctions For example theend-Permian extinction event aftermath is not generally thought tohave exceeded 5Myr and was significantly less in the case of me-tazoan-rich reefs which appeared within 15Myr (Brayard et al 2011)

In reviewing factors to explain the prolonged lsquoresurgence of mi-crobialites and the absence of reef-building metazoansrsquo during the mid-Cambrian to early Ordovician Rowland and Shapiro (2002 p116ndash120) concluded that nutrient deficiency elevated levels of CO2 andtemperature (including associated reduction in oxygen availability)and lower levels of MgCa ratio in seawater could have been involvedWebby (2002) recognized that Ordovician low oxygen prolonged mi-crobial carbonates and slowed metazoan diversification until the LateOrdovician Increased bioturbation has been related to the return ofwidespread anoxic and sometimes euxinic conditions in the earlyndashmidPaleozoic ocean (Boyle et al 2014 Lenton et al 2014) and Saltzmanet al (2015) noted that the Cambrian and Ordovician radiations areseparated by persistent oceanic anoxia and elevated extinction ratesPruss et al (2010) linked the scarcity of calcified skeletons in Fur-ongianndashTremadocian seas in which subsurface water masses werelsquocommonly dysoxic to anoxicrsquo to reduction in carbonate saturationThis interpretation of lowered saturation for CaCO3 minerals in surfacewaters during episodes of anoxia stems from efforts to account for thescarcity of ldquorobust skeletonsrdquo during the Early Triassic (Fischer et al2007 Knoll et al 2007) Since anaerobic microbial processes can in-crease alkalinity it has been suggested that times when deep anoxicseawater was geologically widespread could have had higher carbonatesaturation (Ω) that promoted seafloor precipitation of CaCO3 mineralsand that under these conditions of increased subsurface alkalinity lsquotheΩ of overlying surface waters should be reducedrsquo (Higgins et al 2009)Accordingly Knoll and Fischer (2011 pp 75 78) suggested that thelimited quantity of hypercalcified organisms (lsquomassively calcifyingsponges and cnidarians and calcareous algaersquo) and metazoan reefs inlate Cambrian and earliest Ordovician oceans may at least in part

reflect depressed carbonate saturation in surface seawater A difficultywith this interpretation is that such low carbonate saturation in shallowwater should also have inhibited the formation of microbial carbonatesand oolites yet these deposits dominate many late CambrianndashearlyOrdovician successions including those examined by Pruss et al(2010)

Widespread and protracted hypoxia can critically affect the phy-siology of marine animals We suggest that lithistids were more tolerantof low oxygen conditions than archaeocyaths and also than most of theskeletal reef builders that flourished in the Middle to Late Ordovicianconsistent with the mid-Cambrian to early Ordovician persistence oflithistid sponges Subsequent invertebrate diversification and microbialcarbonate decline during the Ordovician reflect the effects of pro-gressive temperature reduction (Trotter et al 2008 Rasmussen et al2016) and increased ocean ventilation (Young et al 2016 Edwardset al 2017) and oxygenation on metazoan diversification (Figs 1 3 47) Tolerance of hypoxia by lithistids and microbes could thereforeaccount for the LSM communitys persistence during the greenhouseperiod of the early Paleozoic

55 Overview

The pattern of early skeletal reef development outlined here com-menced with Cloudina ~550Ma in the late Ediacaran and continueduntil large stromatoporoid-coral reefs appeared ~465Ma in theDarriwilian We recognize six reef intervals during this time (Fig 8) ILate Ediacaran (~550ndash541Ma) reefs contain Cloudina up to 15 cm insize Namacalathus up to 35 cm and Namapoikia (although apparentlylimited to fissures) up to 1m in extent These organisms have not beenrecognized in the Paleozoic II So far as is known reefs of the earliestCambrian (Fortunianndashmid-Age 2) lack skeletal metazoans except forldquoLadathecardquo worms III Archaeocyath sponges from mid-Age 2 towithin Age 4 commonly up to 15 cm in size locally constructed rela-tively large frameworks (Fig 4) IV Late Age 4 to Age 10 lithistidsponges and the reefs they constructed were both initially relativelysmall (Figs 4 5) but increased in size in the late Cambrian (Age 10) VAdditions to lithistids in Early Ordovician reefs include cup-like ca-lathiids bryozoans Amsassia Lichenaria Cystostroma and PulchrilaminaWith the possible exception of Namapoikia the latter four may re-present the earliest massive laminar-domical skeletal reef-buildersThus from midndashlate Cambrian to early Ordovician lithistid-microbialreefs appear to show progressive increase (Figs 3 4) in sponge size andreef size as well as in diversity with the addition of non-lithistid reef-builders VI This interval commenced in the late Darriwilian with theappearance of stromatoporoid-coral-bryozoan reefs (Webby 2002)

These various EdiacaranndashOrdovician reefs are all potentially frame-reefs in the sense of Riding (2002) Their metazoan skeletons are tub-ular coniform globular domical and laminar in outline and all ap-pear to have been capable at least partially of mutual attachment(Pitcher 1964 Rowland 1984 Riding and Zhuravlev 1995 Pennyet al 2014 Hong et al 2015 Li et al 2015 Lee et al 2016a)Nonetheless vertical-oriented forms (tubular coniform globular) re-quire either mutual support or matrix (including microbial carbonate)support whereas laminar to domical forms are more able to create theirown stability (Kroumlger et al 2017) Thus EdiacaranndashOrdovician reefbuilding skeletons shift from dependence on matrix andor frameworksupport (erect tubular globular coniform) prior to the Early Ordovi-cian to self-stabilizing encrusting laminar-domical forms (tabulatecorals bryozoans stromatoporoids) in the mid-Ordovician

Numerous areas for investigation arise from this overview of earlyPhanerozoic skeletal reef-building organisms Much remains to be dis-covered concerning the affinities ecology and history of Ediacaranorganisms such as Cloudina Namacalathus and Namapoikia These ap-pear to have suffered end-Ediacaran extinction (Amthor et al 2003)but the apparent scarcity of reef-building animals in the earliest Cam-brian requires confirmation Similar questions of affinity and history

surround Cambrian coralomorphs and the early history of lithistids isalso unclear The earliest recorded lithistid Rankenella from near theearlyndashmiddle Cambrian boundary (Kruse 1996) does not appear to bereefal The earliest known reef-building lithistid is Rankenella zhang-xianensis in the upper part of Stage 5 of Cambrian Series 3 (Lee et al2016a) Our focus on the midndashlate Cambrian draws attention to en-vironmental changes associated with archaeocyath decline in lateEpoch 2 as well as those linked to reef diversification in the Trema-docian It also directs attention toward lithistid reef abundance withinthe last 25Myrs of the Cambrian Most of the examples we emphasizehere have been discovered or described since 2003 (Table 1) Certainlymany more remain to be discovered and will provide new insights intothis neglected group and their reef-building abilities Similarly recentprogress in understanding coralomorphs bryozoans tabulates pul-chrilaminids and stromatoporoids is important in assessing how la-minardomical morphotypes contributed to and changed reefs duringthe Ordovician Commonly overlooked groups such as radiocyathsreceptaculitids and cyclocrinitids are locally probably more significantreef components than is generally realized and deserve more attentionIn this review we have often mentioned but not emphasized the sig-nificant role of microbial carbonates as major reef components asso-ciated with these skeletal organisms throughout the late Ediacaran to

mid-Ordovician Competitive and mutualistic relationships betweenthese closely associated but very different components provide fertileground for research to elucidate substrate evolution and reef-buildingstrategies at the dawn of the Phanerozoic Not least our emphasis of thesignificance of marine oxygenation and its spatial and temporal pat-terns during this interval raises numerous unresolved and temptingquestions at the interfaces of geochemistry geobiology and sedi-mentology

6 Conclusions

Cambrian reefs were dominated by microbial carbonates (stroma-tolites dendrolites thrombolites) together with either calcareous (ar-chaeocyath) or siliceous (lithistid) sponges capable of constructing in-terconnected skeletal frameworks Heavily calcified archaeocyaths arerelatively conspicuous in early Cambrian reefs Following their declinemicrobial carbonates continued to dominate reefs and the midndashlateCambrian was regarded as a significant gap in metazoan reef devel-opment However it is now recognized that lithistid sponges arewidespread in midndashlate Cambrian reefs Although easy to overlook andoften subordinate to microbial carbonates lithistids built frameworkssimilar to archaeocyaths This lithistid-microbial reef consortium

~521 ~509 ~497 4854

Drumian Pai-bian

Jiang-shanian Tremadocian FloianGuzhan

-gian Age 10Age 5Age 4Age 3Age 2

541 470

Fortunian

loudina-Namacalathus

4584 Ma

DarriwilianDapin-gian

II III IV V VI

domical(coralomorphs)

coniform-globular

(archaeocyaths radiocyaths)

coniform(lithistidsCalathium)

domical-laminar(pulchrilaminidsstromatoporoids

bryozoans corals)

archaeocyath

Calathium

cnidarian coralomorph

pulchrilaminid

pelmatozoan

bryozoan

radiocyath

lithistid

Cloudina

stromatoporoid

chaetetid

cribricyath

tubular

lsquoLadathecarsquoNamacalathus Namapoikia

Reef Interval I

Terreneuvian Epoch 2 Epoch 3 Furongian Early OrdovicianEdiacaran

Middle Ordovician

Fig 8 Size patterns of late Ediacaran to Middle Ordovician reef-building skeletal organisms based on examples in Supplementary Table 1 Three major morphotypesare emphasized tubular coniform-globular domical-laminar Tubular Cloudina and ldquoLadathecardquo occur in the late Ediacaran and early Cambrian respectivelyConiform sponges (archaeocyaths lithistids Calathium) augmented by globular radiocyaths are locally conspicuous in Cambrian and Early Ordovician reefsDomical-laminar forms are represented by coralomorphs in Cambrian Age 2ndash4 and by pulchrilaminids stromatoporoids bryozoans and corals in the OrdovicianThese data suggest peaks in skeletal reef-builder size in Reef Interval III and in Reef Intervals V and VI with smaller skeletons during Reef Interval IV Reef intervalsI microbial-Cloudina II microbial-ldquoLadathecardquo III microbial-archaeocyath IV microbial-lithistid V microbial-lithistid-calathiid-pulchrilaminid VI stromato-poroid-bryozoan-tabulate-receptaculitid-microbial

continued into the Early Ordovician when lithistids became more di-verse and reef-building was significantly augmented by bryozoans ta-bulate corals and sponges such as the archaeocyath-like Calathium andstromatoporoid-like Pulchrilamina This Early Ordovician reef associa-tion can be seen as a transition from Cambrian lithistid-microbial reefsto the bryozoan-tabulate coral-stromatoporoid reefs that flourished inthe late Darriwilian ~460Ma Subsequently these relatively large andheavily calcified skeletons many of which are laminar to domical inoverall morphology continued to dominate reef-building for~100Myr until the Late Devonian

Geochemical evidence suggests that rise in marine oxygenationduring the EdiacaranndashCambrian transition was not maintained and wasfollowed during the midndashlate Cambrian by a widespread tendency tomarine hypoxia-dysoxia This supports the long-established inferencethat black shale intervals linked to episodes of Cambrian trilobite ex-tinction reflect widespread anoxia It is also consistent with the viewthat midndashlate Cambrian ldquogreenhouserdquo conditions with temperaturesincreased by elevated CO2 led to marine stratification that reducedoxygen availability Extensive carbonate platforms that developed inresponse to increased CO2 temperature and sea-level are likely to havefurther restricted shallow-marine circulation in the midndashlate Cambrianand Early Ordovician

Many present-day silicified sponges including lithistids are well-adapted to low oxygen conditions as are microbes whereas corals andbryozoans generally are not The midndashlate Cambrian development andpersistence of lithistid-microbial reefs could therefore reflect a pro-longed tendency to low oxygen conditions in shallow marine environ-ments Oxygen limitation may have caused the decline of late earlyCambrian archaeocyaths and also hindered their subsequent recoveryIt is likely to have delayed the diversification of reef builders such asbryozoans and corals The tendency toward marine hypoxia continuedfor at least 25Myr until the end of the Cambrian Its gradual ameli-oration in the Early Ordovician can be linked to decline in sea-surfacetemperatures that promoted ocean ventilation The addition ofbryozoans tabulates and stromatoporoids to lithistid-microbial reefs inthe Early Ordovician reflects progressive marine oxygenation Lithistid-microbial reefs did not disappear but their period of early Paleozoicdominance was at an end by the late Darriwilian Nonetheless nearly

300Myr later during the Middle to Late Jurassic a similar lithistid-microbial reef community reappeared in low-oxygen marine environ-ments

Marine oxygenation likely stimulated EdiacaranndashCambrian diversi-fication but ldquogreenhouserdquo conditions subsequently reduced oxygenavailability in shallow reefal environments delaying midndashlateCambrian metazoan diversification and prolonging development oflithistid-microbial reefs (Fig 9) Marine oxygen level could thereforehave been a key factor that initially facilitated early Cambrian di-versification and then ndash as oxygenation declined ndash restrained its sub-sequent advance until the Ordovician This two-step tempo parallelingthat of coeval animal evolution in general could account for the pro-longed pause between the Cambrian Explosion and the GOBE

Acknowledgements

We thank Jackson Chu and Henry Reiswig for advice regardingsponge ecology Keun-Hyung Choi for information concerning ar-thropod oxygen requirements and Liyuan Liang for calculating thedissolved oxygen values in Fig 7 together with the Supplemental DataWe are indebted to three reviewers for valuable comments and sug-gestions and to Andreacute Strasser for expert editorial guidance and en-couragement JHLs research was supported by National ResearchFoundation of Korea (grant 2016R1C1B1012104) This study is a con-tribution to IGCP Project 653 lsquoThe onset of the Great Ordovician Bio-diversity Eventrsquo

Appendix A Supplementary data

Supplementary data to this article can be found online at httpsdoiorg101016jearscirev201804003

References

Adachi N Ezaki Y Liu J 2011 Early Ordovician shift in reef construction from mi-crobial to metazoan reefs PALAIOS 26 106ndash114 httpdxdoiorg102110palo2010p10-097r

Adachi N Ezaki Y Liu J 2012 The oldest bryozoan reefs a unique Early Ordovicianskeletal framework construction Lethaia 45 14ndash23 httpdxdoiorg101111j

4438 Ma

Late Ordovician

Terreneuvian~521 ~509 ~497 4854

Ediacaran

microbial-Cloudina

Middle Ordovician

Epoch 2 Epoch 3

Fig 9 Schematic patterns of EdiacaranndashOrdovician skeletal reef structure and marine oxygenation based on data summarized here (see Figs 1 2 7) Microbial-archaeocyath reefs include domical coralomorphs Marine oxygenation is inferred to have stimulated reef diversification into and including the early Cambrianwhereas reduced oxygen availability in midndashlate Cambrian reef environments is reflected by development of lithistid-microbial reefs This continued with addition ofcalathiids and pulchrilaminids into the early Ordovician Increased marine oxygenation in the midndashlate Ordovician stimulated further and significant diversificationof reef organisms setting the scene for much of the Silurian and Devonian

1502-3931201100268xAdachi N Kotani A Ezaki Y Liu J 2015 Cambrian Series 3 lithistid spongendashmi-

crobial reefs in Shandong Province North China reef development after the dis-appearance of archaeocyaths Lethaia 48 405ndash416 httpdxdoiorg101111let12118

Ader M Sansjofre P Halverson GP Busigny V Trindade RIF Kunzmann MNogueira ACR 2014 Ocean redox structure across the Late NeoproterozoicOxygenation Event a nitrogen isotope perspective Earth Planet Sci Lett 396 1ndash13httpdxdoiorg101016jepsl201403042

Adrain JM McAdams NEB Westrop SR 2009 Trilobite biostratigraphy and revisedbases of the Tulean and Blackhillsian stages of the Ibexian Series Lower Ordovicianwestern United States Memoirs of the Association of Australasian Palaeontologists37 541ndash610

Alberstadt LP Walker KR Zurawski RP 1974 Patch reefs in the Carters Limestone(Middle Ordovician) in Tennessee and vertical zonation in Ordovician reefs GeolSoc Am Bull 85 1171ndash1182 httpdxdoiorg1011300016-7606(1974)85lt1171PRITCLgt20CO2

Algeo TJ Meyers PA Robinson RS Rowe H Jiang GQ 2014Icehousendashgreenhouse variations in marine denitrification Biogeosciences 111273ndash1295 httpdxdoiorg105194bg-11-1273-2014

Allison PA Wells MR 2006 Circulation in large ancient epicontinental seas whatwas different and why PALAIOS 21 513ndash515 httpdxdoiorg102110palo2006S06

Allison PA Wright VP 2005 Switching off the carbonate factory A-tidality strati-fication and brackish wedges in epeiric seas Sediment Geol 179 175ndash184 httpdxdoiorg101016jsedgeo200505004

Altieri AH Harrison SB Seemann J Collin R Diaz RJ Knowlton N 2017Tropical dead zones and mass mortalities on coral reefs Proc Natl Acad Sci 1143660ndash3665 httpdxdoiorg101073pnas1621517114

Amthor JE Grotzinger JP Schroumlder S Bowring SA Ramezani J Martin MWMatter A 2003 Extinction of Cloudina and Namacalathus at the Precambrian-Cambrian boundary in Oman Geology 31 431ndash434 httpdxdoiorg1011300091-7613(2003)031lt0431EOCANAgt20CO2

Antcliffe JB Callow RH Brasier MD 2014 Giving the early fossil record of spongesa squeeze Biol Rev 89 972ndash1004 httpdxdoiorg101111brv12090

Austin T 1845 Note on Mr Bowerbanks paper on the genus Dunstervillia (Bowerbank)with remarks on the Ischadites Koumlnigii the Tentaculites and the Conularia Ann MagNat Hist 15 406ndash407

Azmy K Stouge S Brand U Bagnoli G Ripperdan R 2014 High-resolution che-mostratigraphy of the CambrianndashOrdovician GSSP enhanced global correlation toolPalaeogeogr Palaeoclimatol Palaeoecol 409 135ndash144 httpdxdoiorg101016jpalaeo201405010

Azmy K Kendall B Brand U Stouge S Gordon GW 2015 Redox conditions acrossthe CambrianndashOrdovician boundary elemental and isotopic signatures retained inthe GSSP carbonates Palaeogeogr Palaeoclimatol Palaeoecol 440 440ndash454 httpdxdoiorg101016jpalaeo201509014

Baars C Ghobadi Pour M Atwood RC 2012 The earliest rugose coral Geol Mag150 371ndash380 httpdxdoiorg101017s0016756812000829

Babcock LE Peng S-C Brett CE Zhu M-Y Ahlberg P Bevis M Robison RA2015 Global climate sea level cycles and biotic events in the Cambrian PeriodPalaeoworld 24 5ndash15 httpdxdoiorg101016jpalwor201503005

Bambach RK 2006 Phanerozoic biodiversity mass extinctions Annu Rev Earth PlanetSci 34 127ndash155 httpdxdoiorg101146annurevearth33092203122654

Bambach RK Knoll AH Sepkoski Jr JJ 2002 Anatomical and ecological con-straints on Phanerozoic animal diversity in the marine realm Proc Natl Acad Sci99 6854ndash6859 httpdxdoiorg101073pnas092150999

Bambach RK Knoll AH Wang SC 2004 Origination extinction and mass deple-tions of marine diversity Paleobiology 30 522ndash542 httpdxdoiorg1016660094-8373(2004)030lt0522OEAMDOgt20CO2

Bassett-Butt L 2016 Systematics biostratigraphy and biogeography of brachiopods andother fossils from the middle Cambrian Nelson Limestone Antarctica GFF 138377ndash392 httpdxdoiorg1010801103589720151094510

Bayer R Riley J Donahue D 1998 The effect of dissolved oxygen level on the weightgain and shell hardness of new-shell American lobster Homarus americanus J WorldAquacult Soc 29 491ndash493 httpdxdoiorg101111j1749-73451998tb00674x

Beadle SC 1988 Dasyclads cyclocrinitids and receptaculitids comparative mor-phology and paleoecology Lethaia 21 1ndash12 httpdxdoiorg101111j1502-39311988tb01745x

Bedford R Bedford WR 1934 New species of Archaeocyathinae and other organismsfrom the Lower Cambrian of Beltana South Australia In Memoirs of the KyancuttaMuseum 1 pp 1ndash7

Bengston S 2004 Early skeletal fossils In Paleontological Society Papers 10 pp67ndash78 httpdxdoiorg101017S1089332600002345

Berkner LV Marshall LC 1965 On the origin and rise of oxygen concentration in theEarths atmosphere J Atmos Sci 22 225ndash261 httpdxdoiorg1011751520-0469(1965)022lt0225OTOAROgt20CO2

Berner RA 1990 Atmospheric carbon dioxide levels over Phanerozoic time Science249 1382ndash1386 httpdxdoiorg101126science24949751382

Berner RA 2009 Phanerozoic atmospheric oxygen new results using theGEOCARBSULF model Am J Sci 309 603ndash606 httpdxdoiorg10247507200903

Berry WBN Wilde P 1978 Progressive ventilation of the oceans-an explanation forthe distribution of the Lower Paleozoic black shales Am J Sci 278 257ndash275

Berry WBN Wilde P Quinby-Hunt MS Orth CJ 1986 Trace element signatures inDictyonema Shales and their geochemical and stratigraphic significance Nor GeolTidsskr 66 45ndash51

Berry WBN Wilde P Quinby-Hunt MS 1989 Paleozoic (Cambrian throughDevonian) anoxitropic biotopes Palaeogeogr Palaeoclimatol Palaeoecol 74 3ndash13httpdxdoiorg1010160031-0182(89)90016-3

Billings E 1865 Palaeozoic fossils Geol Surv Canada 208ndash211Bolton TE Copeland MJ 1963 Cambrotrypa and Bradoria from the Middle Cambrian

of western Canada J Paleontol 1069ndash1070Bond GC Kominz MA Steckler MS Grotzinger JP 1989 Role of thermal sub-

sidence flexure and eustasy in the evolution of Early Paleozoic passive-margincarbonate platforms In Crevello PD Wilson JL Sarg JF Read JF (Eds)Controls on Carbonate Platform and Basin Development SEPM Special Publication44 Tulsa pp 39ndash61

Bowring SA Grotzinger JP Isachsen CE Knoll AH Pelechaty SM Kolosov P1993 Calabrating rates of Early Cambrian evolution Science 261 1293ndash1298httpdxdoiorg101126science11539488

Boyle RA Dahl TW Dale AW Shields-Zhou GA Zhu M Brasier MD CanfieldDE Lenton TM 2014 Stabilization of the coupled oxygen and phosphorus cyclesby the evolution of bioturbation Nat Geosci 7 671ndash676 httpdxdoiorg101038ngeo2213

Brasier M Green O Shields G 1997 Ediacarian sponge spicule clusters from south-western Mongolia and the origins of the Cambrian fauna Geology 25 303ndash306httpdxdoiorg1011300091-7613(1997)025lt0303esscfsgt23co2

Brayard A Vennin E Olivier N Bylund KG Jenks J Stephen DA Bucher HHofmann R Goudemand N Escarguel G 2011 Transient metazoan reefs in theaftermath of the end-Permian mass extinction Nat Geosci 4 694ndash697 httpdxdoiorg101038ngeo1264

Brett CE Liddell WD Derstler KL 1983 Late Cambrian hard substrate communitiesfrom MontanaWyoming the oldest known hardground encrusters Lethaia 16281ndash289 httpdxdoiorg101111j1502-39311983tb02010x

Bruumlck WM Reed JK McCarthy PJ 2012 The bacterial community of the lithistidsponge Discodermia spp as determined by cultivation and culture-independentmethods Mar Biotechnol 14 762ndash773 httpdxdoiorg101007s10126-012-9443-6

Brunton FR Dixon OA 1994 Siliceous sponge-microbe biotic associations and theirrecurrence through the Phanerozoic as reef mound constructors PALAIOS 9370ndash387 httpdxdoiorg1023073515056

Buchardt B Lewan MD 1990 Reflectance of vitrinite-like macerals as a thermalmaturity index for Cambrian-Ordovician Alum Shale southern Scandinavia AAPGBull 74 394ndash406

Byrnes JG 1968 Notes on the nature and environmental significance of theReceptaculitaceae Lethaia 1 368ndash381

Cantildeas F Carrera M 1993 Early Ordovician microbial-sponge-receptaculitid biohermsof the Precordillera western Argentina Facies 29 169ndash178 httpdxdoiorg101007BF02536927

Canfield DE Poulton SW Narbonne GM 2007 Late-Neoproterozoic deep-oceanoxygenation and the rise of animal life Science 315 92ndash95 httpdxdoiorg101126science1135013

Canfield DE Poulton SW Knoll AH Narbonne GM Ross G Goldberg T StraussH 2008 Ferruginous conditions dominated later Neoproterozoic deep-waterchemistry Science 321 949ndash952 httpdxdoiorg101126science1154499

Carrera MG Astini RA Gomez FJ 2017 A lowermost Ordovician tabulate-likecoralomorph from the Precordillera of western Argentina a main component of areef-framework consortium J Paleontol 91 73ndash85 httpdxdoiorg101017jpa2016145

Chen X Ling HF Vance D Shields-Zhou GA Zhu M Poulton SW Och LMJiang SY Li D Cremonese L Archer C 2015 Rise to modern levels of oceanoxygenation coincided with the Cambrian radiation of animals Nat Commun 67142 httpdxdoiorg101038ncomms8142

Cheng M Li C Zhou L Feng L Algeo TJ Zhang F Romaniello S Jin C LingH Jiang S 2017 Transient deep-water oxygenation in the early Cambrian NanhuaBasin South China Geochim Cosmochim Acta 210 42ndash58 httpdxdoiorg101016jgca201704032

Chu JW Tunnicliffe V 2015 Oxygen limitations on marine animal distributions andthe collapse of epibenthic community structure during shoaling hypoxia GlobChang Biol 21 2989ndash3004 httpdxdoiorg101111gcb12898

Church SB 1974 Lower Ordovician patch reefs in western Utah Brigham Young UnivGeol Stud 21 41ndash62

Church SB 1991 A new Lower Ordovician species of Calathium and skeletal structuresof western Utah calathids J Paleontol 65 602ndash610 httpdxdoiorg101017S0022336000030699

Church SB 2009 Problematic receptaculitid fossils from western Utah and easternNevada In Tripp BT Krahulec K Jordan JL (Eds) Geology and GeologicResources and Issues of Western Utah Utah Geological Association Publication Vol38 pp 55ndash66

Church SB 2017 Efficient ornamentation in Ordovician anthaspidellid spongesPaleontol Contrib 18 1ndash8

Cloud PE 1948 Some problems and patterns of evolution exemplified by fossil in-vertebrates Evolution 2 322ndash350 httpdxdoiorg101111j1558-56461948tb02750x

Cohen KM Finney SC Gibbard PL Fan J-X 2013 The ICS international chron-ostratigraphic chart Episodes 36 199ndash204

Conway Morris S 1986 The community structure of the Middle Cambrian PhyllopodBed (Burgess Shale) Palaeontology 29 423ndash467

Conway Morris S 2006 Darwins dilemma the realities of the Cambrian lsquoexplosionrsquoPhilos Trans R Soc Lon B Biol Sci 361 1069ndash1083 httpdxdoiorg101098rstb20061846

Conway Morris S Mattes BW Chen M 1990 The early skeletal organism Cloudinanew occurrences from Oman and possibly China Am J Sci 290-A 245ndash260

Conway KW Barrie JV Austin WC Luternauer JL 1991 Holocene sponge bio-herms on the western Canadian continental shelf Cont Shelf Res 11 771ndash790httpdxdoiorg1010160278-4343(91)90079-L

Copper P 1974 Structure and development of early Paleozoic reefs In Proceedings ofthe Second International Coral Reef Symposium pp 365ndash386

Copper P 2001 Evolution radiations and extinctions in Proterozoic to mid-Paleozoic

reefs In Stanley GD (Ed) The History and Sedimentology of Ancient Reef SystemsKluwer AcademicPlenum Publishers New York pp 89ndash119 httpdxdoiorg101007978-1-4615-1219-6_3

Coulson KP Brand LR 2016 Lithistid sponge-microbial reef-building communitiesconstruct laminated upper Cambrian (Furongian) stromatolites PALAIOS 31358ndash370 httpdxdoiorg102110palo2016029

Cremonese L Shields-Zhou GA Struck U Ling H-F Och LM 2014 Nitrogen andorganic carbon isotope stratigraphy of the Yangtze platform during theEdiacaranndashCambrian transition in South China Palaeogeogr PalaeoclimatolPalaeoecol 398 165ndash186 httpdxdoiorg101016jpalaeo201312016

Cuffey RJ Zhu Z 2010 Yichang (Central China)ndashthe oldest-known bryozoan reefs(mid-Early Ordovician) and comparison with the next-oldest (Garden Island NewYorkVermont early Middle Ordovician) Geol Soc Am Abstr Programs 42 64

Cuffey RJ Chuantao X Zhu Z Spjeldnaes N Hu Z-X 2013 The worlds oldest-known bryozoan reefs late Tremadocian mid-Early Ordovician Yichang CentralChina In Ernst A Schaumlfer P Scholz J (Eds) Bryozoan Studies 2010 Springer-Verlag BerlinHeidelberg pp 13ndash27 httpdxdoiorg101007978-3-642-16411-8_2

Dahl TW Hammarlund EU Anbar AD Bond DP Gill BC Gordon GW KnollAH Nielsen AT Schovsbo NH Canfield DE 2010 Devonian rise in atmo-spheric oxygen correlated to the radiations of terrestrial plants and large predatoryfish Proc Natl Acad Sci 107 17911ndash17915 httpdxdoiorg101073pnas1011287107

Dahl TW Boyle RA Canfield DE Connelly JN Gill BC Lenton TM BizzarroM 2014 Uranium isotopes distinguish two geochemically distinct stages during thelater Cambrian SPICE event Earth Planet Sci Lett 401 313ndash326 httpdxdoiorg101016jepsl201405043

Dattilo BF Hlohowskyj S Ripperdan RL Miller JF Shapiro RS 2004Stratigraphic setting of an Upper Cambrian metazoan reef between the NopahFormation to Goodwin Formation transition in southern Nevada Geol Soc AmAbstr Programs 36 368

de Freitas TA Trettin HP Dixon OA Mallamo M 1999 Silurian System of theCanadian Arctic Archipelago Bull Can Petrol Geol 47 136ndash193

Debrenne F Reitner J 2001 Sponges cnidarians and ctenophores In Zhuravlev AYRiding R (Eds) Ecology of the Cambrian Radiation Columbia University PressNew York pp 301ndash325

Debrenne F Termier H Termier G 1970 Radiocyatha Une nouvelle classe dorga-nismes primitifs du Cambrien infeacuterieur Bulletin de la Socieacuteteacute Geacuteologique de France12 120ndash125 (in French)

Debrenne F Rozanov AY Webers GF 1984 Upper Cambrian Archaeocyatha fromAntarctica Geol Mag 121 291ndash299 httpdxdoiorg101017S0016756800029186

Debrenne FM Gangloff RA Lafuste JG 1987 Tabulaconus Handfield micro-structure and its implication in the taxonomy of primitive corals J Paleontol 611ndash9 httpdxdoiorg101017S0022336000028122

Debrenne F Zhuravlev AY Kruse PD 2015a Archaeocyatha and Cribricyatha no-mina nuda taxa not Archaeocyatha Radiocyatha or Cribricyatha In Stearn CW(Ed) Treatise on Invertebrate Paleontology Part E Porifera Revised HypercalcifiedPorifera Volumes 4 and 5 The University of Kansas Paleontological InstituteLawrence Kansas pp 1105ndash1106

Debrenne F Zhuravlev AY Kruse PD 2015b General Features of the ArchaeocyathaIn Stearn CW (Ed) Treatise on Invertebrate Paleontology Part E PoriferaRevised Hypercalcified Porifera Volumes 4 and 5 The University of KansasPaleontological Institute Lawrence Kansas pp 845ndash922

Desrochers A James NP 1989 Middle Ordovician (Chazyan) bioherms and bios-tromes of the Mingan Islands Quebec In Geldsetzer HHJ James NP TebbuttGE (Eds) Reefs Canada and adjacent areas Canadian Society of PetroleumGeologists Memoir 13 Canadian Society of Petroleum Geologists pp 183ndash191

Drosdova NA 1980 Algae in the Lower Cambrian organogenous buildups of westernMongolia In Transactions of the Joint Soviet-Mongolian Paleontological Expedition10 pp 1ndash140 (in Russian)

Droser ML Sheehan PM 1997 Palaeoecology of the Ordovician radiation resolutionof large-scale patterns with individual clade histories palaeogeography and en-vironments Geobios 20 221ndash229 httpdxdoiorg101016S0016-6995(97)80027-7

Edwards CT Saltzman MR Leslie SA Bergstroumlm SM Sedlacek ARC HowardA Bauer JA Sweet WC Young SA 2015 Strontium isotope (87Sr86Sr) stra-tigraphy of Ordovician bulk carbonate implications for preservation of primaryseawater values Geol Soc Am Bull 127 1275ndash1289 httpdxdoiorg101130b311491

Edwards CT Saltzman MR Royer DL Fike DA 2017 Oxygenation as a driver ofthe Great Ordovician Biodiversification Event Nat Geosci 10 925ndash929 httpdxdoiorg101038s41561-017-0006-3

Egenhoff SO Fishman NS Ahlberg P Maletz J Jackson A Kolte K Lowers HMackie J Newby W Petrowsky M 2015 Sedimentology of SPICE (Steptoeanpositive carbon isotope excursion) a high-resolution trace fossil and microfabricanalysis of the middle to late Cambrian Alum Shale Formation southern Sweden InLarsen D Egenhoff SO Fishman NS (Eds) Paying Attention to MudrocksPriceless Geological Society of America Special Paper 515 Geological Society ofAmerica pp 87ndash102 httpdxdoiorg10113020152515_05

Ekau W Auel H Poumlrtner HO Gilbert D 2010 Impacts of hypoxia on the structureand processes in pelagic communities (zooplankton macro-invertebrates and fish)Biogeosciences 7 1669ndash1699 httpdxdoiorg105194bg-7-1669-2010

Elias RJ Lee D-J Woo S-K 2008 Corallite increase and mural pores in Lichenaria(Tabulata Ordovician) J Paleontol 82 377ndash390 httpdxdoiorg10166606-1141

Erbacher J Huber BT Norris RD Markey M 2001 Increased thermohaline stra-tification as a possible cause for an ocean anoxic event in the Cretaceous periodNature 409 325ndash327 httpdxdoiorg10103835053041

Erwin DH Laflamme M Tweedt S Sperling EA Pisani D Peterson KJ 2011

The Cambrian conundrum early divergence and later ecological success in the earlyhistory of animals Science 334 1091ndash1097 httpdxdoiorg101126science1206375

Fagerstrom JA 1987 The Evolution of Reef Communities John Wiley and Sons NewYork (600 pp)

Faggetter LE Wignall PB Pruss SB Newton RJ Sun Y Crowley SF 2017Trilobite extinctions facies changes and the ROECE carbon isotope excursion at theCambrian series 2ndash3 boundary Great Basin western USA PalaeogeogrPalaeoclimatol Palaeoecol 478 53ndash66 httpdxdoiorg101016jpalaeo201704009

Fan L Reynolds D Liu M Stark M Kjelleberg S Webster NS Thomas T 2012Functional equivalence and evolutionary convergence in complex communities ofmicrobial sponge symbionts Proc Natl Acad Sci 109 E1878ndashE1887 httpdxdoiorg101073pnas1203287109

Fike DA Grotzinger JP Pratt LM Summons RE 2006 Oxidation of the Ediacaranocean Nature 444 744ndash747 httpdxdoiorg101038nature05345

Finks RM Toomey DF 1969 The paleoecology of Chazyan (lower Middle Ordovician)reefs or mounds State University College of Arts and Sciences Plattsburg NewYork State Geological Association Field Guide Book pp 93ndash120

Fischer AG 1984 The two Phanerozoic supercycles In Berggren WA Van CouveringJA (Eds) Catastrophes and Earth History The New Uniformitarianism PrincetonUniversity Press Princeton NJ pp 129ndash150

Fischer WW Higgins JA Pruss SB 2007 Delayed biotic recovery from thePermianndashTriassic extinction may have been influenced by a redox-driven re-organization of the marine carbonate system Geol Soc Am Abstr Programs 39420

Fortey R 2000 Olenid trilobites the oldest known chemoautotrophic symbionts ProcNatl Acad Sci 97 6574ndash6578 httpdxdoiorg101073pnas97126574

Frakes LA Francis JE Syktus JI 1992 Climate modes of the PhanerozoicCambridge University Press (274 pp)

Fritz MA 1947 Cambrian Bryozoa J Paleontol 21 434ndash435Fritz MA 1948 Cambrian Bryozoa more precisely dated J Paleontol 22 373Fritz MA Howell BF 1955 An Upper Cambrian coral from Montana J Paleontol 29

181ndash183Fritz MA Howell BF 1959 Cambrotrypa montanensis a Middle Cambrian fossil of

possible coral affinities Proc Geol Assoc Canada 11 89ndash93Fuller MK Jenkins RJF 1994 Moorowipora chamberensis a coral from the Early

Cambrian Moorowie Formation Flinders Ranges South Australia Trans R Soc SAust 118 227ndash235

Fuller MK Jenkins RJF 1995 Arrowipora fromensis a new genus of tabulate-like coralfrom the Early Cambrian Moorowie Formation Flinders Ranges South AustraliaTrans R Soc S Aust 119 75ndash82

Fuller M Jenkins R 2007 Reef corals from the Lower Cambrian of the Flinders RangesSouth Australia Palaeontology 50 961ndash980 httpdxdoiorg101111j1475-4983200700682x

Fuumlrsich FT Werner W 1991 Palaeoecology of coralline sponge-coral meadows fromthe Upper Jurassic of Portugal Palaumlontol Z 65 35ndash69 httpdxdoiorg101007BF02985773

Fyffe LR Pickerill RK 1993 Geochemistry of Upper Cambrian-Lower Ordovicianblack shale along a northeastern Appalachian transect Geol Soc Am Bull 105897ndash910 httpdxdoiorg1011300016-7606(1993)105lt0897GOUCLOgt23CO2

Gaines RR 2014 Burgess Shale-type preservation and its distribution in space and timeIn Laflamme M Schiffbauer JD Darroch SAF (Eds) Reading and Writing ofthe Fossil Record Preservational Pathways to Exceptional Fossilization ThePaleontological Society Papers 20 The Paleontological Society pp 123ndash146

Gaines RR Droser ML 2010 The paleoredox setting of Burgess Shale-type depositsPalaeogeogr Palaeoclimatol Palaeoecol 297 649ndash661 httpdxdoiorg101016jpalaeo201009014

Gaines RR Kennedy MJ Droser ML 2005 A new hypothesis for organic pre-servation of Burgess Shale taxa in the middle Cambrian Wheeler Formation HouseRange Utah Palaeogeogr Palaeoclimatol Palaeoecol 220 193ndash205 httpdxdoiorg101016jpalaeo200407034

Gandin A Debrenne F 2010 Distribution of the archaeocyath-calcimicrobial biocon-structions on the Early Cambrian shelves Palaeoworld 19 222ndash241 httpdxdoiorg101016jpalwor201009010

Gehling JG Rigby JK 1996 Long expected sponges from the Neoproterozoic Ediacarafauna of South Australia J Paleontol 70 185ndash195 httpdxdoiorg101017S0022336000023283

Gerhardt AM Gill BC 2016 Elucidating the relationship between the later Cambrianend-Marjuman extinctions and SPICE event Palaeogeogr Palaeoclimatol Palaeoecol461 362ndash373 httpdxdoiorg101016jpalaeo201608031

Germs GJB 1972 New shelly fossils from Nama Group South West Africa Am J Sci272 752ndash761 httpdxdoiorg102475ajs2728752

Geyer G Bayet-Goll A Wilmsen M Mahboubi A Moussavi-Harami R 2014Lithostratigraphic revision of the middle Cambrian (Series 3) and upper Cambrian(Furongian) in northern and Central Iran Newsl Stratigr 47 21ndash59 httpdxdoiorg1011270078-042120140039

Gill BC Lyons TW Saltzman MR 2007 Parallel high-resolution carbon and sulfurisotope records of the evolving Paleozoic marine sulfur reservoir PalaeogeogrPalaeoclimatol Palaeoecol 256 156ndash173 httpdxdoiorg101016jpalaeo200702030

Gill BC Lyons TW Young SA Kump LR Knoll AH Saltzman MR 2011Geochemical evidence for widespread euxinia in the later Cambrian ocean Nature469 80ndash83 httpdxdoiorg101038nature09700

Glass LM Phillips D 2006 The Kalkarindji continental flood basalt province a newCambrian large igneous province in Australia with possible links to faunal extinc-tions Geology 34 461ndash464 httpdxdoiorg101130g221221

Goldberg T Poulton S Strauss H 2005 Sulphur and oxygen isotope signatures of lateNeoproterozoic to early Cambrian sulphate Yangtze Platform China diagenetic

constraints and seawater evolution Precambrian Res 137 223ndash241 httpdxdoiorg101016jprecamres200503003

Grotzinger JP Watters WA Knoll AH 2000 Calcified metazoans in thrombolite-stromatolite reefs of the terminal Proterozoic Nama Group Namibia Paleobiology26 334ndash359 httpdxdoiorg1016660094-8373(2000)026lt0334CMITSRgt20CO2

Guilbaud R Slater BJ Poulton SW Harvey THP Brocks JJ Nettersheim BJButterfield NJ 2018 Oxygen minimum zones in the early Cambrian OceanGeochem Persp Lett 33ndash38 httpdxdoiorg107185geochemlet1806

Gunda VG Janapala VR 2009 Effects of dissolved oxygen levels on survival andgrowth in vitro of Haliclona pigmentifera (Demospongiae) Cell Tissue Res 337527ndash535 httpdxdoiorg101007s00441-009-0843-5

Guo Q Strauss H Liu C Zhao Y Yang X Peng J Yang H 2010 A negativecarbon isotope excursion defines the boundary from Cambrian Series 2 to CambrianSeries 3 on the Yangtze Platform South China Palaeogeogr PalaeoclimatolPalaeoecol 285 143ndash151 httpdxdoiorg101016jpalaeo200911005

Halverson GP Wade BP Hurtgen MT Barovich KM 2010 Neoproterozoic che-mostratigraphy Precambrian Res 182 337ndash350 httpdxdoiorg101016jprecamres201004007

Hamdi B Rozanov AY Zhuravlev AY 1995 Latest Middle Cambrian metazoan reeffrom northern Iran Geol Mag 132 367ndash373 httpdxdoiorg101017S0016756800021439

Harper DAT 2006 The Ordovician biodiversification setting an agenda for marinelife Palaeogeogr Palaeoclimatol Palaeoecol 232 148ndash166 httpdxdoiorg101016jpalaeo200507010

Hentschel U Piel J Degnan SM Taylor MW 2012 Genomic insights into themarine sponge microbiome Nat Rev Microbiol 10 641ndash654 httpdxdoiorg101038nrmicro2839

Hicks M 2006 A new genus of early Cambrian coral in Esmeralda County southwesternNevada J Paleontol 80 609ndash615 httpdxdoiorg1016660022-3360(2006)80[609ANGOEC]20CO2

Higgins JA Fischer WW Schrag DP 2009 Oxygenation of the ocean and sedimentsconsequences for the seafloor carbonate factory Earth Planet Sci Lett 284 25ndash33httpdxdoiorg101016jepsl200903039

Hill D 1964 The phylum Archaeocyatha Biol Rev 39 232ndash258 httpdxdoiorg101111j1469-185X1964tb00956x

Hill MS Hill AL Lopez J Peterson KJ Pomponi S Diaz MC Thacker RWAdamska M Boury-Esnault N Cardenas P Chaves-Fonnegra A Danka E DeLaine BO Formica D Hajdu E Lobo-Hajdu G Klontz S Morrow CC Patel JPicton B Pisani D Pohlmann D Redmond NE Reed J Richey S Riesgo ARubin E Russell Z Rutzler K Sperling EA di Stefano M Tarver JE CollinsAG 2013 Reconstruction of family-level phylogenetic relationships withinDemospongiae (Porifera) using nuclear encoded housekeeping genes PLoS One 8e50437 httpdxdoiorg101371journalpone0050437

Hinde GJ 1883 Catalogue of the Fossil Sponges in the Geological Department of theBritish Museum (Natural History) With Descriptions of New and Little-KnownSpecies Taylor and Francis London (237 pp)

Hoffmann F Schlaumlppy M-L 2011 Sponges (Porifera) and sponge microbes In ThielV (Ed) J Reitner Springer Encyclopedia of Geobiology pp 840ndash847 httpdxdoiorg101007978-1-4020-9212-1_194

Hoffmann F Larsen O Thiel V Rapp HT Pape T Michaelis W Reitner J 2005An anaerobic world in sponges Geomicrobiol J 22 1ndash10 httpdxdoiorg10108001490450590922505

Hofmann HJ Mountjoy EW 2001 Namacalathus-Cloudina assemblage inNeoproterozoic Miette Group (Byng Formation) British Columbia Canadas oldestshelly fossils Geology 29 1091ndash1094 httpdxdoiorg1011300091-7613(2001)029(1091NCAINM)20CO2

Hong J Cho S-H Choh S-J Woo J Lee D-J 2012 Middle Cambrian siliceoussponge-calcimicrobe buildups (Daegi Formation Korea) metazoan buildup con-stituents in the aftermath of the Early Cambrian extinction event Sediment Geol253ndash254 47ndash57 httpdxdoiorg101016jsedgeo201201011

Hong J Choh S-J Lee D-J 2014 Tales from the crypt early adaptation of crypto-biontic sessile metazoans PALAIOS 29 95ndash100 httpdxdoiorg102110palo2014076

Hong J Choh S-J Lee D-J 2015 Untangling intricate microbialndashsponge frame-works the contributions of sponges to Early Ordovician reefs Sediment Geol 31875ndash84 httpdxdoiorg101016jsedgeo201501003

Hong J Lee J-H Choh S-J Lee D-J 2016 Cambrian Series 3 carbonate platform ofKorea dominated by microbial-sponge reefs Sediment Geol 341 58ndash69 httpdxdoiorg101016jsedgeo201604012

Hong J Choh S-J Park J Lee D-J 2017 Construction of the earliest stromato-poroid framework labechiid reefs from the Middle Ordovician of Korea PalaeogeogrPalaeoclimatol Palaeoecol 470 54ndash62 httpdxdoiorg101016jpalaeo201701017

Hong J Oh J-R Lee J-H Choh S-J Lee D-J 2018 The earliest evolutionary linkof metazoan bioconstruction laminar stromatoporoidndashbryozoan reefs from theMiddle Ordovician of Korea Palaeogeogr Palaeoclimatol Palaeoecol 492 126ndash133httpdxdoiorg101016jpalaeo201712018

Hough ML Shields GA Evins LZ Strauss H Henderson RA Mackenzie S 2006A major sulphur isotope event at c 510 ma a possible anoxia-extinction-volcanismconnection during the Early-Middle Cambrian transition Terra Nova 18 257ndash263httpdxdoiorg101111j1365-3121200600687x

Huang J Zou C Li J Dong D Wang S Wang S Cheng K 2012 Shale gasgeneration and potential of the Lower Cambrian Qiongzhusi Formation in thesouthern Sichuan Basin China Pet Explor Dev 39 75ndash81 httpdxdoiorg101016s1876-3804(12)60017-2

Hurtgen MT Pruss SB Knoll AH 2009 Evaluating the relationship between thecarbon and sulfur cycles in the later Cambrian Ocean an example from the Port auPort Group western Newfoundland Canada Earth Planet Sci Lett 281 288ndash297httpdxdoiorg101016jepsl200902033

Imhoff JF Truumlper HG 1976 Marine sponges as habitats of anaerobic phototrophicbacteria Microb Ecol 3 1ndash9 httpdxdoiorg101007BF02011449

Irwin ML 1965 General theory of epeiric clear water sedimentation AAPG Bull 49445ndash459

James NP Kobluk DR 1978 Lower Cambrian patch reefs and associated sedimentssouthern Labrador Canada Sedimentology 25 1ndash35 httpdxdoiorg101111j1365-30911978tb00299x

James NP Wood R 2010 Reefs In James NP Dalrymple RW (Eds) FaciesModels 4 Geological Association of Canada St Johns pp 421ndash447

Jell JS 1984 Cambrian cnidarians with mineralized skeletons Palaeontogr Am 54105ndash109

Jenkyns HC 1991 Impact of Cretaceous sea level rise and anoxic events on theMesozoic carbonate platform of Yugoslavia AAPG Bull 75 1007ndash1017 httpdxdoiorg1013060c9b28ad-1710-11d7-8645000102c1865d

Jenkyns HC 2010 Geochemistry of oceanic anoxic events Geochem Geophys Geosyst11 Q03004 httpdxdoiorg1010292009gc002788

Jenkyns HC Schouten-Huibers L Schouten S Damsteacute JSS 2012 Warm MiddleJurassic-Early Cretaceous high-latitude sea-surface temperatures from the southernocean Clim Past 8 215ndash226 httpdxdoiorg105194cp-8-215-2012

Jiang SY Pi DH Heubeck C Frimmel H Liu YP Deng HL Ling HF YangJH 2009 Early Cambrian ocean anoxia in South China Nature 459 E5-6 discussionE6 httpsdoiorg101038nature08048

Jin C Li C Algeo TJ Planavsky NJ Cui H Yang X Zhao Y Zhang X Xie S2016 A highly redox-heterogeneous ocean in South China during the early Cambrian(sim529ndash514Ma) implications for biota-environment co-evolution Earth Planet SciLett 441 38ndash51 httpdxdoiorg101016jepsl201602019

Johns RA Dattilo BF Spincer B 2007 Neotype and redescription of the UpperCambrian anthaspidellid sponge Wilbernicyathus donegani Wilson 1950 J Paleontol81 435ndash444 httpdxdoiorg101666050281

Jourdan F Hodges K Sell B Schaltegger U Wingate MTD Evins LZ SoderlundU Haines PW Phillips D Blenkinsop T 2014 High-precision dating of theKalkarindji large igneous province Australia and synchrony with the Early-MiddleCambrian (Stage 4-5) extinction Geology 42 543ndash546 httpdxdoiorg101130g354341

Kah LC Bartley JK 2011 Protracted oxygenation of the Proterozoic biosphere IntGeol Rev 53 1424ndash1442 httpdxdoiorg101080002068142010527651

Kah LC Thompson CK Henderson MA Zhan R 2016 Behavior of marine sulfur inthe Ordovician Palaeogeogr Palaeoclimatol Palaeoecol 458 133ndash153 httpdxdoiorg101016jpalaeo201512028

Kapp US 1975 Paleoecology of Middle Ordovician stromatoporoid mounds inVermont Lethaia 8 195ndash207 httpdxdoiorg101111j1502-39311975tb00923x

Kasting JF Howard MT Wallmann K Veizer J Shields G Jaffreacutes J 2006Paleoclimates ocean depth and the oxygen isotopic composition of seawater EarthPlanet Sci Lett 252 82ndash93 httpdxdoiorg101016jepsl200609029

Keeling RE Kortzinger A Gruber N 2010 Ocean deoxygenation in a warming worldAnnu Rev Mar Sci 2 199ndash229 httpdxdoiorg101146annurevmarine010908163855

Keller M Fluumlgel E 1996 Early Ordovician reefs from Argentina Stromatoporoid vsStromatolite origin Facies 34 177ndash192 httpdxdoiorg101007BF02546163

Kelly M 2007 Porifera Lithistid Demospongiae (Rock Sponges) In NIWA BiodiversityMemoir 121 Graphic Press amp Packaging Ltd Levin (100 pp)

Kendall B Komiya T Lyons TW Bates SM Gordon GW Romaniello SJ JiangG Creaser RA Xiao S McFadden K Sawaki Y Tahata M Shu D Han J LiY Chu X Anbar AD 2015 Uranium and molybdenum isotope evidence for anepisode of widespread ocean oxygenation during the late Ediacaran period GeochimCosmochim Acta 156 173ndash193 httpdxdoiorg101016jgca201502025

Kershaw S 2015 Paleoecology of the Paleozoic Stromatoporoidea In Stearn CW(Ed) Treatise on Invertebrate Paleontology Part E Porifera Revised HypercalcifiedPorifera Volumes 4 and 5 The University of Kansas Paleontological InstituteLawrence Kansas pp 631ndash651

Kesling RV Graham A 1962 Ischadites is a Dasycladacean alga J Paleontol 36943ndash952

Kiessling W 2009 Geologic and biologic controls on the evolution of reefs Annu RevEcol Evol Syst 40 173ndash192 httpdxdoiorg101146annurevecolsys110308120251

Klappa CF James NP 1980 Small lithistid sponge bioherms early Middle OrdovicianTable Head Group western Newfoundland Bull Can Petrol Geol 28 425ndash451

Knight I Azmy K Boyce WD Lavoie D 2008 Tremadocian carbonate rocks of thelower St George Group Port au Port Peninsula western Newfoundland lithostrati-graphic setting of diagenetic isotopic and geochemistry studies In GeologicalSurvey Report 08ndash1 Newfoundland and Labrador Department of Natural Resourcespp 115ndash149

Knoll AH 2003 Biomineralization and evolutionary history Rev Mineral Geochem54 329ndash356 httpdxdoiorg1021130540329

Knoll AH 2011 The multiple origins of complex multicellularity Annu Rev EarthPlanet Sci 39 217ndash239 httpdxdoiorg101146annurevearth031208100209

Knoll AH Carroll SB 1999 Early animal evolution emerging views from comparativebiology and geology Science 284 2129ndash2137 httpdxdoiorg101126science28454232129

Knoll AH Fischer WW 2011 Skeletons and ocean chemistry the long view InGattuso J-P Hansson L (Eds) Ocean Acidification Oxford University PressOxford pp 67ndash82

Knoll AH Bambach RK Payne JL Pruss S Fischer WW 2007 Paleophysiologyand end-Permian mass extinction Earth Planet Sci Lett 256 295ndash313 httpdxdoiorg101016jepsl200702018

Kobluk DR 1979 A new and unusual skeletal organism from the Lower Cambrian ofLabrador Can J Earth Sci 16 2040ndash2045 httpdxdoiorg101139e79-189

Kobluk DR 1984 A new compound skeletal organism from the Rosella Formation(Lower Cambrian) Atan Group Cassiar Mountains British Columbia J Paleontol

58 703ndash708Kroumlger B Hints L Lehnert O 2014 Age facies and geometry of the SandbianKatian

(Upper Ordovician) pelmatozoan-bryozoan-receptaculitid reefs of the VasalemmaFormation northern Estonia Facies 60 963ndash986 httpdxdoiorg101007s10347-014-0410-8

Kroumlger B Desrochers A Ernst A 2017 The reengineering of reef habitats during theGreat Ordovician Biodiversification Event PALAIOS 32 584ndash599 httpdxdoiorg102110palo2017017

Kruse PD 1983 Middle Cambrian lsquoArchaeocyathusrsquo from the Georgina Basin is an an-thaspidellid sponge Alcheringa 7 49ndash58 httpdxdoiorg10108003115518308619633

Kruse PD 1996 Update on the northern Australian Cambrian sponges RankenellaJawonya and Wagima Alcheringa 20 161ndash178 httpdxdoiorg10108003115519608619188

Kruse PD Reitner JR 2014 Northern Australian microbial-metazoan reefs after themid-Cambrian mass extinction Memoirs of the Association of AustralasianPalaeontologists 45 31ndash53

Kruse PD Zhuravlev AY 2008 Middle-Late Cambrian Rankenella-Girvanella reefs ofthe Mila Formation northern Iran Can J Earth Sci 45 619ndash639 httpdxdoiorg101139e08-016

Kruse PD Zhuravlev AY James NP 1995 Primordial metazoan-calcimicrobialreefs Tommotian (Early Cambrian) of the Siberian platform PALAIOS 10 291ndash321httpdxdoiorg1023073515157

Kruse PD Gandin A Debrenne F Wood R 1996 Early Cambrian bioconstructionsin the Zavkhan Basin of western Mongolia Geol Mag 133 429ndash444 httpdxdoiorg101017S0016756800007597

Kruse PD Zhuravlev AY Debrenne F 2015 Radiocyaths and potentially allied taxaIn Stearn CW (Ed) Treatise on Invertebrate Paleontology Part E PoriferaRevised Hypercalcified Porifera Volumes 4 and 5 The University of KansasPaleontological Institute Lawrence Kansas pp 1085ndash1093

Lafuste J Debrenne F Gandin A Gravestock D 1991 The oldest tabulate coral andthe associated Archaeocyatha Lower Cambrian Flinders Ranges South AustraliaGeobios 24 697ndash718 httpdxdoiorg101016S0016-6995(06)80298-6

Landing E 1993 In situ earliest Cambrian tube worms and the oldest metazoan-con-structed biostrome (Placentian Series southeastern Newfoundland) J Paleontol 67333ndash342 httpdxdoiorg101017s0022336000036817

Landing E 2012a The Great American Carbonate Bank in eastern Laurentia its birthsdeaths and linkage to paleooceanic oxygenation (Early Cambrian ndash Late Ordovician)In Derby JR Fritz RD Longacre SA Morgan WA Sternbach CA (Eds) TheGreat American Carbonate Bank The Geology and Economic Resources of theCambrian-Ordovician Sauk Megasequence of Laurentia AAPG Memoir 98 AAPG pp451ndash492 httpdxdoiorg10130613331502M983502

Landing E 2012b Time-specific black mudstones and global hyperwarming on theCambrianndashOrdovician slope and shelf of the Laurentia palaeocontinent PalaeogeogrPalaeoclimatol Palaeoecol 367ndash368 256ndash272 httpdxdoiorg101016jpalaeo201109005

Landing E English A Keppie JD 2010 Cambrian origin of all skeletalized metazoanphylamdashdiscovery of Earths oldest bryozoans (Upper Cambrian southern Mexico)Geology 38 547ndash550 httpdxdoiorg101130g308701

Landing E Antcliffe JB Brasier MD English AB 2015 Distinguishing Earthsoldest known bryozoan (Pywackia late Cambrian) from pennatulacean octocorals(MesozoicndashRecent) J Paleontol 89 292ndash317 httpdxdoiorg101017jpa201426

Laub RS 1984 Lichenaria Winchell amp Schuchert 1895 Lamottia Raymond 1924 andthe early history of the tabulate corals In Oliver WA Sando WJ Cairns SDCoates AG Macintyre IG Bayer FM Sorauf JE (Eds) Recent Advances in thePaleobiology and Geology of the Cnidaria Palaeontographica Americana Vol 54 pp159ndash163

Lavoie D Desrochers A Dix G Knight I Hersi OS 2012 The Great AmericanCarbonate Bank in Eastern Canada an overview In Derby JR Fritz RDLongacre SA Morgan WA Sternbach CA (Eds) The Great American CarbonateBank the Geology and Economic Resources of the Cambrian-Ordovician SaukMegasequence of Laurentia AAPG memoir 98 AAPG httpdxdoiorg10130613331504M983503

Lavy A Keren R Yahel G Ilan M 2016 Intermittent hypoxia and prolonged suboxiameasured in situ in a marine sponge Front Mar Sci 3 263 httpdxdoiorg103389fmars201600263

Lee J-H Riding R 2016 Marine hypoxia lithistid sponge-microbial communities andthe cause of the Cambrian reef gap In 26th Goldschmidt Conference 1699

Lee J-H Chen J Choh S-J Lee D-J Han Z Chough SK 2014a Furongian (lateCambrian) sponge-microbial maze-like reefs in the North China platform PALAIOS29 27ndash37 httpdxdoiorg102110palo2013050

Lee J-H Lee HS Chen J Woo J Chough SK 2014b Calcified microbial reefs inthe Cambrian Series 2 of the North China Platform implications for the evolution ofCambrian calcified microbes Palaeogeogr Palaeoclimatol Palaeoecol 403 30ndash42httpdxdoiorg101016jpalaeo201403020

Lee M Sun N Choh S-J Lee D-J 2014c A new Middle Ordovician reef assemblagefrom north-Central China and its palaeobiogeographical implications SedimentGeol 310 30ndash40 httpdxdoiorg101016jsedgeo201405003

Lee J-H Chen J Chough SK 2015a The middlendashlate Cambrian reef transition andrelated geological events a review and new view Earth Sci Rev 145 66ndash84 httpdxdoiorg101016jearscirev201503002

Lee J-H Chen J Woo J 2015b The earliest Phanerozoic carbonate hardground(Cambrian Stage 5 Series 3) implications to the paleoseawater chemistry and earlyadaptation of hardground fauna Palaeogeogr Palaeoclimatol Palaeoecol 440172ndash179 httpdxdoiorg101016jpalaeo201507043

Lee J-H Hong J Choh S-J Lee D-J Woo J Riding R 2016a Early recovery ofsponge framework reefs after Cambrian archaeocyath extinction ZhangxiaFormation (early Cambrian Series 3) Shandong North China PalaeogeogrPalaeoclimatol Palaeoecol 457 269ndash276 httpdxdoiorg101016jpalaeo2016

06018Lee J-H Hong J Lee D-J Choh S-J 2016b A new Middle Ordovician bivalvendash-

siliceous spongendashmicrobe reef-building consortium from North China PalaeogeogrPalaeoclimatol Palaeoecol 457 23ndash30 httpdxdoiorg101016jpalaeo201605034

Lee J-H Kim B-J Liang K Park T-Y Choh S-J Lee D-J Woo J 2016cCambrian reefs in the western North China platform Wuhai Inner Mongolia ActaGeol Sin 90 1946ndash1954 httpdxdoiorg1011111755-672413014

Lee J-H Woo J Lee D-J 2016d The earliest reef-building anthaspidellid spongeRankenella zhangxianensis n sp from the Zhangxia Formation (Cambrian Series 3)Shandong Province China J Paleontol 90 1ndash9 httpdxdoiorg101017jpa201553

Leggett JK 1980 British Lower Palaeozoic black shales and their palaeo-oceanographicsignificance J Geol Soc Lond 137 139ndash156 httpdxdoiorg101144gsjgs13720139

Leinfelder RR 2001 Jurassic reef ecosystems In Stanley GD (Ed) The History andSedimentology of Ancient Reef Systems Kluwer AcademicPlenum Publishers NewYork pp 251ndash309 httpdxdoiorg101007978-1-4615-1219-6_8

Leinfelder RR Krautter M Laternser D-GR Nose M Schmid DU Schweigert GWerner W Keupp H Brugger D-GH Herrmann R Rehfeld-Kiefer USchroeder JH Reinhold C Koch R Zeiss A Schweizer V Christmann HMenges G Luterbacher H 1994 The origin of Jurassic reefs current researchdevelopments and results Facies 31 1ndash56 httpdxdoiorg101007BF02536932

Leinfelder RR Werner W Nose M Schmid DU Krautter M Laternser R TakacsM Hartmann D 1996 Paleoecology growth parameters and dynamics of coralsponge and microbolite reefs from the Late Jurassic In Reitner J Neuweiler FGunkel F (Eds) Global and Regional Controls on Biogenic Sedimentation 1 ReefEvolution Research Reports Goumlttinger Arbeiten zur Geologie und PalaumlontologieSonderband 2 Goumlttingen pp 227ndash248

Leinfelder RR Schmid DU Nose M Werner W 2002 Jurassic reef patternsmdashtheexpression of a changing globe In Kiessling W Fluumlgel E Golonka J (Eds)Phanerozoic Reef Patterns SEPM Tulsa pp 465ndash520 SEPM special publication 72httpsdoiorg102110pec02720465

Lenton TM Boyle RA Poulton SW Shields-Zhou GA Butterfield NJ 2014 Co-evolution of eukaryotes and ocean oxygenation in the Neoproterozoic era NatGeosci 7 257ndash265 httpdxdoiorg101038ngeo2108

Leacutevi C 1991 Lithistid sponges from the Norfolk Rise Recent and Mesozoic genera InReitner J Keupp H (Eds) Fossil and Recent Sponges Springer Berlin pp 72ndash82httpdxdoiorg101007978-3-642-75656-6_7

Levin LA Ekau W Gooday AJ Jorissen F Middelburg JJ Naqvi SWA NeiraC Rabalais NN Zhang J 2009 Effects of natural and human-induced hypoxia oncoastal benthos Biogeosciences 6 2063ndash2098 httpdxdoiorg105194bg-6-2063-2009

Li C-W Chen J-Y Hua T-E 1998 Precambrian sponges with cellular structuresScience 279 879ndash882 httpdxdoiorg101126science2795352879

Li Q Li Y Kiessling W 2014 Early Ordovician sponge-Calathium-microbial reefs onthe Yangtze Platform margin of the South China Block GFF 136 157ndash161 httpdxdoiorg101080110358972013862852

Li Q Li Y Wang J Kiessling W 2015 Early Ordovician lithistid spongendashCalathiumreefs on the Yangtze Platform and their paleoceanographic implicationsPalaeogeogr Palaeoclimatol Palaeoecol 425 84ndash96 httpdxdoiorg101016jpalaeo201502034

Li C Jin C Planavsky NJ Algeo TJ Cheng M Yang X Zhao Y Xie S 2017aCoupled oceanic oxygenation and metazoan diversification during the earlyndashmiddleCambrian Geology 45 743ndash746 httpdxdoiorg101130g392081

Li Q Li Y Kiessling W 2017b The oldest labechiid stromatoporoids from in-traskeletal crypts in lithistid sponge-Calathium reefs Lethaia 50 140ndash148 httpdxdoiorg101111let12182

Li Q Li Y Zhang Y Munnecke A 2017c Dissecting Calathium-microbial frame-works the significance of calathids for the Middle Ordovician reefs in the TarimBasin northwestern China Palaeogeogr Palaeoclimatol Palaeoecol 474 66ndash78httpdxdoiorg101016jpalaeo201608005

Liu B Rigby JK Zhu Z 2003 Middle Ordovician lithistid sponges from the Bachu-Kalpin area Xinjiang northwestern China J Paleontol 77 430ndash441 httpdxdoiorg1016660022-3360(2003)077lt0430molsftgt20co2

Loch JD Stitt JH Derby JR 1993 Cambrian-Ordovician boundary interval ex-tinctions implications of revised trilobite and brachiopod data from Mount WilsonAlberta Canada J Paleontol 67 497ndash517 httpdxdoiorg101017S0022336000024859

Love GD Grosjean E Stalvies C Fike DA Grotzinger JP Bradley AS Kelly AEBhatia M Meredith W Snape CE Bowring SA Condon DJ Summons RE2009 Fossil steroids record the appearance of Demospongiae during the Cryogenianperiod Nature 457 718ndash721 httpdxdoiorg101038nature07673

Luo C Reitner J 2014 First report of fossil keratose demosponges in Phanerozoiccarbonates preservation and 3-D reconstruction Naturwissenschaften 101 467ndash477httpdxdoiorg101007s00114-014-1176-0

Ma J Taylor PD Xia F Zhan R Sevastopulo G 2015 The oldest known bryozoanProphyllodictya (Cryptostomata) from the lower Tremadocian (Lower Ordovician) ofLiujiachang south-western Hubei central China Palaeontology 58 925ndash934 httpdxdoiorg101111pala12189

Maldonado M Aguilar R Blanco J Garcia S Serrano A Punzon A 2015Aggregated clumps of lithistid sponges a singular reef-like bathyal habitat withrelevant paleontological connections PLoS One 10 e0125378 httpdxdoiorg101371journalpone0125378

Maldonado M Aguilar R Bannister RJ Bell JJ Conway KW Dayton PK DiacuteazC Gutt J Kelly M Kenchington ELR Leys SP Pomponi SA Rapp HTRuumltzler K Tendal OS Vacelet J Young CM 2016 Sponge grounds as keymarine habitats a synthetic review of types structure functional roles and con-servation concerns In Rossi S Bramanti L Gori A Orejas C (Eds) MarineAnimal Forests The Ecology of Benthic Biodiversity Hotspots Springer Cham pp

1ndash39 httpdxdoiorg101007978-3-319-17001-5_24-1Maloof AC Porter SM Moore JL Dudas FO Bowring SA Higgins JA Fike

DA Eddy MP 2010a The earliest Cambrian record of animals and ocean geo-chemical change Geol Soc Am Bull 122 1731ndash1774 httpdxdoiorg101130b303461

Maloof AC Rose CV Beach R Samuels BM Calmet CC Erwin DH PoirierGR Yao N Simons FJ 2010b Possible animal-body fossils in pre-Marinoanlimestones from South Australia Nat Geosci 3 653ndash659 httpdxdoiorg101038ngeo934

Marenco PJ Martin KR Marenco KN Barber DC 2016 Increasing global oceanoxygenation and the Ordovician radiation insights from ThU of carbonates from theOrdovician of western Utah Palaeogeogr Palaeoclimatol Palaeoecol 458 77ndash84httpdxdoiorg101016jpalaeo201605014

Markello JR Read JF 1981 Carbonate ramp-to-deeper shale shelf transitions of anUpper Cambrian intrashelf basin Nolichucky Formation Southwest VirginiaAppalachians Sedimentology 28 573ndash597 httpdxdoiorg101111j1365-30911981tb01702x

Matabos M Tunnicliffe V Juniper SK Dean C 2012 A year in hypoxia epibenthiccommunity responses to severe oxygen deficit at a subsea observatory in a coastalinlet PLoS One 7 e45626 httpdxdoiorg101371journalpone0045626

McKenzie NR Hughes NC Gill BC Myrow PM 2014 Plate tectonic influences onNeoproterozoic-early Paleozoic climate and animal evolution Geology 42 127ndash130httpdxdoiorg101130g349621

Mentel M Rottger M Leys S Tielens AG Martin WF 2014 Of early animalsanaerobic mitochondria and a modern sponge BioEssays 36 924ndash932 httpdxdoiorg101002bies201400060

Mi J Zhang S Chen J Tang L He Z 2007 The distribution of the oil derived fromCambrian source rocks in Lunnan area the Tarim Basin China Chin Sci Bull 52133ndash140 httpdxdoiorg101007s11434-007-6004-x

Middleburg JJ Levin LA 2009 Coastal hypoxia and sediment biogeochemistryBiogeosciences 6 1273ndash1293 httpdxdoiorg105194bg-6-1273-2009

Miller KG Kominz MA Browning JV Wright JD Mountain GS Katz MESugarman PJ Cramer BS Christie-Blick N Pekar SF 2005 The Phanerozoicrecord of global sea-level change Science 310 1293ndash1298 httpdxdoiorg101126science1116412

Miller JF Evans KR Dattilo BF 2012 The Great American Carbonate Bank in themiogeocline of western central Utah tectonic influences on sedimentation In DerbyJR Fritz RD Longacre SA Morgan WA Sternbach CA (Eds) The GreatAmerican Carbonate Bank The Geology and Economic Resources of the Cambrian-Ordovician Sauk Megasequence of Laurentia AAPG Memoir 98 AAPG pp 769ndash854httpdxdoiorg10130613331516M983498

Mills DB Canfield DE 2014 Oxygen and animal evolution did a rise of atmosphericoxygen trigger the origin of animals BioEssays 36 1145ndash1155 httpdxdoiorg101002bies201400101

Mills DB Ward LM Jones C Sweeten B Forth M Treusch AH Canfield DE2014 Oxygen requirements of the earliest animals Proc Natl Acad Sci 1114168ndash4172 httpdxdoiorg101073pnas1400547111

Montantildeez IP Osleger DA Banner JL Mack LE Musgrove M 2000 Evolution ofthe Sr and C isotope composition of Cambrian oceans GSA Today 10 1ndash5

Morgan WA 2012 Sequence stratigraphy of the Great American Carbonate Bank InDerby JR Fritz RD Longacre SA Morgan WA Sternbach CA (Eds) TheGreat American Carbonate Bank The Geology and Economic Resources of theCambrian-Ordovician Sauk Megasequence of Laurentia AAPG Memoir 98 AAPG pp37ndash82 httpdxdoiorg10130613331499M980271

Morrow C Caacuterdenas P 2015 Proposal for a revised classification of the Demospongiae(Porifera) Front Zool 12 7 httpdxdoiorg101186s12983-015-0099-8

Mrozek S Dattilo BF Hicks M Miller JF 2003 Metazoan reefs from the UpperCambrian of the Arrow Canyon Range Clark County Nevada Geol Soc Am AbstrPrograms 35 500

Mundy DJC 1994 Microbialite-sponge-bryozoan-coral framestones in LowerCarboniferous (Late Visean) buildups of northern England (UK) In Embry AFBeauchamp B Glass DJ (Eds) Pangea Global Environments and Resources CSPGSpecial Publications 17 Canadian Society of Petroleum Geologists Calgary pp713ndash729

Muscente AD Marc Michel F Dale JG Xiao S 2015 Assessing the veracity ofPrecambrian lsquospongersquo fossils using in situ nanoscale analytical techniquesPrecambrian Res 263 142ndash156 httpdxdoiorg101016jprecamres201503010

Myagkova YI 1966 Soanitesmdasha new group of organisms Int Geol Rev 8 795ndash802httpdxdoiorg10108000206816609474340

Na L Kiessling W 2015 Diversity partitioning during the Cambrian radiation ProcNatl Acad Sci 112 4702ndash4706 httpdxdoiorg101073pnas1424985112

Nance RD Murphy JB 2013 Origins of the supercontinent cycle Geosci Front 4439ndash448 httpdxdoiorg101016jgsf201212007

Newell ND 1972 The evolution of reefs Sci Am 226 54ndash69Nitecki MH 1970 North American cyclocrinitid algae In Fieldiana Geology 21

History Field Museum of Natural (182 pp)Nitecki MH 1972 Ischadites abbottae a new North American Silurian species

(Dasycladales) Phycologia 10 263ndash275Nitecki MH Debrenne F 1979 The nature of Radiocyathids and their relationship to

Receptaculitids and Archaeocyathids Geobios 12 5ndash27 httpdxdoiorg101016S0016-6995(79)80106-0

Nitecki MH Mutvei H Nitecki DV 1999 Receptaculitids a phylogenetic debate on aproblematic fossil taxon KluwerPlenum New York (241 pp)

Nitecki MH Webby BD Spjeldnaes N Zhen Y-Y 2004 Receptaculitids and algaeIn Webby BD Paris F Droser ML Percival IG (Eds) The Great OrdovicianBiodiversification Event Columbia University Press New York pp 336ndash347

Nowak H Servais T Monnet C Molyneux SG Vandenbroucke TRA 2015Phytoplankton dynamics from the Cambrian Explosion to the onset of the GreatOrdovician Biodiversification Event a review of Cambrian acritarch diversity Earth

Sci Rev 151 117ndash131 httpdxdoiorg101016jearscirev201509005Och LM Cremonese L Shields-Zhou GA Poulton SW Struck U Ling H Li D

Chen X Manning C Thirlwall M Strauss H Zhu M Fairchild I 2016Palaeoceanographic controls on spatial redox distribution over the Yangtze platformduring the Ediacaran-Cambrian transition Sedimentology 63 378ndash410 httpdxdoiorg101111sed12220

Ogg JG Ogg G Gradstein FM 2016 A concise geologic time scale Elsevier (240 pp)Oliver WA 1996 Origins and relationships of Paleozoic coral groups and the origin of

the Scleractinia Paleontological Society Papers 1 107ndash134Oliver WA Coates AG 1987 Phylum Cnidaria In Boardman RS Cheetham AH

Rowell AJ (Eds) Fossil Invertebrates Blackwell Oxford pp 140ndash193Opalinski PR Harland TL 1981 The Middle Ordovician of the Oslo Region Norway

29 Stratigraphy of the Mjoslashsa Limestone in the Toten and Nes-Hamar areas NorGeol Tidsskr 61 59ndash78

Pacheco ML Galante D Rodrigues F Leme Jde M Bidola P Hagadorn WStockmar M Herzen J Rudnitzki ID Pfeiffer F Marques AC 2015 Insightsinto the skeletonization lifestyle and affinity of the unusual Ediacaran fossilCorumbella PLoS One 10 e0114219 httpdxdoiorg101371journalpone0114219

Pagegraves A Schmid S 2016 Euxinia linked to the Cambrian Drumian carbon isotopeexcursion (DICE) in Australia geochemical and chemostratigraphic evidencePalaeogeogr Palaeoclimatol Palaeoecol 461 65ndash76 httpdxdoiorg101016jpalaeo201608008

Palmer AR 1984 The biomere problem evolution of an idea J Paleontol 58599ndash611

Palmer AR James NP 1979 The Hawke Bay event A circum-Iapetus regression nearthe lower Middle Cambrian boundary In Wones DR (Ed) The Caledonides in theUSA IGCP Project 27 Caledonide orogen Department of Geological SciencesVirginia Polytechnic Institute and State University Blacksburg Virginia pp 15ndash18

Parente M Frijia G Di Lucia M Jenkyns HC Woodfine RG Baroncini F 2008Stepwise extinction of larger foraminifers at the Cenomanian-Turonian boundary ashallow-water perspective on nutrient fluctuations during oceanic anoxic event 2(Bonarelli event) Geology 36 715ndash718 httpdxdoiorg101130g24893a1

Park T-Y Woo J Lee D-J Lee D-C Lee S-B Han Z Chough SK Choi DK2011 A stem-group cnidarian described from the mid-Cambrian of China and itssignificance for cnidarian evolution Nat Commun 2 442 httpdxdoiorg101038ncomms1457

Park T-YS Kihm J-H Woo J Zhen Y-Y Engelbretsen M Hong J Choh S-JLee D-J 2016 Cambrian stem-group cnidarians with a new species from theCambrian Series 3 of the Taebaeksan Basin Korea Acta Geol Sin 90 827ndash837httpdxdoiorg1011111755-672412726

Pashin JC Kopaska-Merkel DC Arnold AC McIntyre MR Thomas WA 2012Gigantic gaseous mushwads in Cambrian shale Conasauga Formation southernAppalachians USA Int J Coal Geol 103 70ndash91 httpdxdoiorg101016jcoal201205010

Pavela JS Ross JL Chittenden ME 1983 Sharp reductions in abundance of fishesand benthic macroinvertebrates in the Gulf of Mexico off Texas associated with hy-poxia Northeast Gulf Sci 6 167ndash173

Payne JL Boyer AG Brown JH Finnegan S Kowalewski M Krause Jr RALyons SK McClain CR McShea DW Novack-Gottshall PM Smith FAStempien JA Wang SC 2009 Two-phase increase in the maximum size of lifeover 35 billion years reflects biological innovation and environmental opportunityProc Natl Acad Sci 106 24ndash27 httpdxdoiorg101073pnas0806314106

Payne JL McClain CR Boyer AG Brown JH Finnegan S Kowalewski M KrauseJr RA Lyons SK McShea DW Novack-Gottshall PM Smith FA Spaeth PStempien JA Wang SC 2011 The evolutionary consequences of oxygenic pho-tosynthesis a body size perspective Photosynth Res 107 37ndash57 httpdxdoiorg101007s11120-010-9593-1

Pedersen TF Calvert SE 1990 Anoxia vs productivity what controls the formationof organic-carbon-rich sediments and sedimentary rocks AAPG Bull 74 454ndash466

Peel JS 2011 The coral Cothonion from the lower Cambrian of North GreenlandAlcheringa 35 405ndash411 httpdxdoiorg101080031155182011521438

Peel JS 2017a The oldest pelmatozoan encrusted hardground and holdfasts fromLaurentia (Cambrian Series 2ndash3) GFF 139 195ndash204 httpdxdoiorg1010801103589720171347196

Peel JS 2017b A problematic cnidarian (Cambroctoconus Octocorallia) from theCambrian (Series 2ndash3) of Laurentia J Paleontol 91 871ndash882 httpdxdoiorg101017jpa201749

Peng S Geyer G Hamdi B 1999 Trilobites from the Shahmirzad section AlborzMountains Iran their taxonomy biostratigraphy and bearing for international cor-relation Beringeria 25 3ndash66

Peng S Babcock LE Cooper RA 2012 The Cambrian Period In Gradstein FMOgg JG Schmitz M Ogg G (Eds) The Geologic Time Scale 2012 Elsevier pp437ndash488 httpdxdoiorg101016b978-0-444-59425-900019-6

Penny AM Wood R Curtis A Bowyer F Tostevin R Hoffman KH 2014Ediacaran metazoan reefs from the Nama Group Namibia Science 344 1504ndash1506httpdxdoiorg101126science1253393

Penny AM Wood RA Zhuravlev AY Curtis A Bowyer F Tostevin R 2017Intraspecific variation in an Ediacaran skeletal metazoan Namacalathus from theNama Group Namibia Geobiology 15 81ndash93 httpdxdoiorg101111gbi12205

Percival LME Witt MLI Mather TA Hermoso M Jenkyns HC Hesselbo SPAl-Suwaidi AH Storm MS Xu W Ruhl M 2015 Globally enhanced mercurydeposition during the end-Pliensbachian extinction and Toarcian OAE a link to theKaroondashFerrar large Igneous Province Earth Planet Sci Lett 428 267ndash280 httpdxdoiorg101016jepsl201506064

Perfetta PJ Shelton KL Stitt JH 1999 Carbon isotope evidence for deep-waterinvasion at the Marjumiid-Pterocephaliid biomere boundary Black Hills USA acommon origin for biotic crises on Late Cambrian shelves Geology 27 403 httpdxdoiorg1011300091-7613(1999)027lt0403ciefdwgt23co2

Peters SE Gaines RR 2012 Formation of the Great Unconformity as a trigger for the

Cambrian explosion Nature 484 363ndash366 httpdxdoiorg101038nature10969Pickett JW Percival IG 2001 Ordovician faunas and biostratigraphy in the

Gunningbland area central New South Wales Australia Alcheringa 25 9ndash52 httpdxdoiorg10108003115510108619212

Pisera A 2002 Fossil Lithistids An Overview In Hooper JNA Van Soest RWM(Eds) Systema Porifera A Guide to the Classification of Sponges Kluwer AcademicPlenum Publishers New York pp 388ndash402

Pisera A Leacutevi C 2002 Lithistid Demospongiae In Hooper JNA Van Soest RWM(Eds) Systema Porifera A Guide to the Classification of Sponges Kluwer AcademicPlenum Publishers New York pp 299ndash301

Pitcher M 1964 Evolution of Chazyan (Ordovician) reefs of eastern United States andCanada Bull Can Petrol Geol 12 632ndash691

Pool W Geluk M Abels J Tiley G Idiz E Leenaarts E 2012 Assessment of anunusual European shale gas play the Cambro-Ordovician Alum Shale southernSweden Proceedings of the Society of Petroleum EngineersEuropean Association ofGeoscientists and Engineers Unconventional Resources Conference Vienna pp152339

Praetorius SK Mix AC Walczak MH Wolhowe MD Addison JA Prahl FG2015 North Pacific deglacial hypoxic events linked to abrupt ocean warming Nature527 362ndash366 httpdxdoiorg101038nature15753

Pratt BR 1989 Small early Middle Ordovician patch reefs Laval Formation (ChazyGroup) Caughnawaga Montreal area Quebec In Geldsetzer HHJ James NPTebbutt GE (Eds) Reefs Canada and adjacent areas Canadian Society ofPetroleum Geologists Memoir 13 Canadian Society of Petroleum Geologists pp218ndash223

Pratt BR James NP 1982 Cryptalgal-metazoan bioherms of early Ordovician age inthe St George Group western Newfoundland Sedimentology 29 543ndash569 httpdxdoiorg101111j1365-30911982tb01733x

Pratt BR Spincer BR Wood RA Zhuravlev AY 2001 Ecology and evolution ofCambrian reefs In Zhuravlev AY Riding R (Eds) Ecology of the CambrianRadiation Columbia University Press New York pp 254ndash274

Pruss SB Knoll AH 2017 Environmental covariation of metazoans and microbialitesin the Lower Ordovician Boat Harbour Formation Newfoundland PalaeogeogrPalaeoclimatol Palaeoecol 485 917ndash929 httpdxdoiorg101016jpalaeo201708007

Pruss SB Finnegan S Fischer WW Knoll AH 2010 Carbonates in skeleton-poorseas new insights from Cambrian and Ordovician strata of Laurentia PALAIOS 2573ndash84 httpdxdoiorg102110palo2009p09-101r

Quinn NJ Kojis BL 1999 Community structure of the living fossil coralline spongepopulations at the Grotto Saipan Northern Mariana Islands Bull Mar Sci 65227ndash234

Rabalais NN Diacuteaz RJ Levin LA Turner RE Gilbert D Zhang J 2010 Dynamicsand distribution of natural and human-caused hypoxia Biogeosciences 7 585ndash619httpdxdoiorg105194bg-7-585-2010

Railsback LB Ackerly SC Anderson TF Cisne JL 1990 Palaeontological andisotope evidence for warm saline deep waters in Ordovician oceans Nature 343156ndash159 httpdxdoiorg101038343156a0

Rasmussen CM Ullmann CV Jakobsen KG Lindskog A Hansen J Hansen TEriksson ME Dronov A Frei R Korte C Nielsen AT Harper DA 2016 Onsetof main Phanerozoic marine radiation sparked by emerging mid Ordovician icehouseSci Rep 6 18884 httpdxdoiorg101038srep18884

Reitner J 1993 Modern cryptic microbialitemetazoan facies from Lizard Island (GreatBarrier Reef Australia) formation and concepts Facies 29 3ndash40 httpdxdoiorg101007BF02536915

Renaud ML 1986 Detecting and avoiding oxygen deficient sea water by brown shrimpPenaeus aztecus (Ives) and white shrimp Penaeus setiferus (Linnaeus) J Exp MarBiol Ecol 98 283ndash292 httpdxdoiorg1010160022-0981(86)90218-2

Rhoads DC Morse JW 1971 Evolutionary and ecologic significance of oxygen-defi-cient marine basins Lethaia 4 413ndash428 httpdxdoiorg101111j1502-39311971tb01864x

Riding R 2001 Calcified algae and bacteria In Zhuravlev AY Riding R (Eds)Ecology of the Cambrian Radiation Columbia University Press New York pp445ndash473

Riding R 2002 Structure and composition of organic reefs and carbonate mud moundsconcepts and categories Earth Sci Rev 58 163ndash231 httpdxdoiorg101016S0012-8252(01)00089-7

Riding R 2004 Solenopora is a chaetetid sponge not an alga Palaeontology 47117ndash122 httpdxdoiorg101111j0031-0239200400351x

Riding R 2006 Microbial carbonate abundance compared with fluctuations in me-tazoan diversity over geological time Sediment Geol 185 229ndash238 httpdxdoiorg101016jsedgeo200512015

Riding R Voronova L 1984 Assemblages of calcareous algae near the PrecambrianCambrian boundary in Siberia and Mongolia Geol Mag 121 205ndash210 httpdxdoiorg101017S0016756800028260

Riding R Zhuravlev AY 1994 Cambrian reef builders calcimicrobes and archae-ocyaths ecological aspects of the Cambrian Radiation IGCP Project 366 Terra NovaCambridge pp 7

Riding R Zhuravlev AY 1995 Structure and diversity of oldest sponge-microbe reefsLower Cambrian Aldan River Siberia Geology 23 649ndash652 httpdxdoiorg1011300091-7613(1995)023(0649SADOOS)23CO2

Riedel B Pados T Pretterebner K Schiemer L Steckbauer A Haselmair AZuschin M Stachowitsch M 2014 Effect of hypoxia and anoxia on invertebratebehaviour ecological perspectives from species to community level Biogeosciences11 1491ndash1518 httpdxdoiorg105194bg-11-1491-2014

Rietschel LS 1977 Receptaculitids are calcareous algae but no dasyclads In Fluumlgel E(Ed) Fossil Algae Recent Results and Developments Springer Berlin HeidelbergBerlin Heidelberg pp 212ndash214 httpdxdoiorg101007978-3-642-66516-5_22

Rietschel S Nitecki MH 1984 Ordovician receptaculitid algae from BurmaPalaeontology 27 415ndash420

Rowland SM 1984 Were there framework reefs in the Cambrian Geology 12

181ndash183 httpdxdoiorg1011300091-7613(1984)12lt181wtfritgt20co2Rowland SM 2001 Archaeocyathsmdasha history of phylogenetic interpretation J

Paleontol 75 1065ndash1078 httpdxdoiorg1016660022-3360(2001)075lt1065AAHOPIgt20CO2

Rowland SM Gangloff RA 1988 Structure and paleoecology of Lower Cambrianreefs PALAIOS 3 111ndash135 httpdxdoiorg1023073514525

Rowland SM Shapiro RS 2002 Reef patterns and environmental influences in theCambrian and earliest Ordovician In Kiessling W Fluumlgel E Golonka J (Eds)Phanerozoic Reef Patterns SEPM Tulsa pp 95ndash128 SEPM special publication 72

Royer DL Berner RA Montantildeez IP Tabor NJ Beerling DJ 2004 CO2 as aprimary driver of Phanerozoic climate GSA Today 14 4ndash10 httpdxdoiorg1011301052-5173(2004)014lt4caapdogt20co2

Rozanov AY Zhuravlev AY 1992 The Lower Cambrian fossil record of the SovietUnion In Lipps JH Signor PW (Eds) Origin and Early Evolution of the MetazoaPlenum Press New York pp 205ndash282

Ryder RT Harris DC Gerome P Hainsworth TJ Burruss RA Lillis PG JarvieDM Pawlewicz MJ 2014 Evidence for Cambrian petroleum source rocks in theRome trough of West Virginia and Kentucky Appalachian basin In Coal andPetroleum Resources in the Appalachian Basin Distribution Geologic Frameworkand Geochemical Character US Geological Survey pp 36 httpdxdoiorg103133pp1708G8

Sahoo SK Planavsky NJ Kendall B Wang X Shi X Scott C Anbar AD LyonsTW Jiang G 2012 Ocean oxygenation in the wake of the Marinoan glaciationNature 489 546ndash549 httpdxdoiorg101038nature11445

Saltzman MR 1999 Upper Cambrian carbonate platform evolution Elvinia andTaenicephalus zones (Pterocephaliid-Ptychaspid biomere boundary) northwesternWyoming J Sediment Res 69 926ndash938 httpdxdoiorg102110jsr69926

Saltzman MR 2005 Phosphorus nitrogen and the redox evolution of the Paleozoicoceans Geology 33 573ndash576 httpdxdoiorg101130g215351

Saltzman MR Davidson JP Holden P Runnegar B Lohmann KC 1995 Sea-level-driven changes in ocean chemistry at an Upper Cambrian extinction horizon Geology23 893ndash896 httpdxdoiorg1011300091-7613(1995)023lt0893SLDCIOgt23CO2

Saltzman MR Ripperdan RL Brasier MD Lohmann KC Robison RA ChangWT Peng S Ergaliev EK Runnegar B 2000 A global carbon isotope excursion(SPICE) during the Late Cambrian relation to trilobite extinctions organic-matterburial and sea level Palaeogeogr Palaeoclimatol Palaeoecol 162 211ndash223 httpdxdoiorg101016s0031-0182(00)00128-0

Saltzman MR Young SA Kump LR Gill BC Lyons TW Runnegar B 2011Pulse of atmospheric oxygen during the late Cambrian Proc Natl Acad Sci 1623876ndash3881 httpdxdoiorg101073pnas1011836108

Saltzman MR Edwards CT Adrain JM Westrop SR 2015 Persistent oceanicanoxia and elevated extinction rates separate the Cambrian and Ordovician radia-tions Geology 43 807ndash810 httpdxdoiorg101130g368141

Savarese M Mount JF Sorauf JE Bucklin L 1993 Paleobiologic and paleoenvir-onmental context of coral-bearing Early Cambrian reefs implications for Phanerozoicreef development Geology 21 917ndash920 httpdxdoiorg1011300091-7613(1993)021(0917PAPCOC)23CO2

Schlanger SO Jenkyns HC 1976 Cretaceous Oceanic Anoxic Events causes andconsequences Geol Mijnb 55 179ndash184

Schlaumlppy ML Schoumlttner SI Lavik G Kuypers MM de Beer D Hoffmann F 2010Evidence of nitrification and denitrification in high and low microbial abundancesponges Mar Biol 157 593ndash602 httpdxdoiorg101007s00227-009-1344-5

Schmitt S Tsai P Bell J Fromont J Ilan M Lindquist N Perez T Rodrigo ASchupp PJ Vacelet J Webster N Hentschel U Taylor MW 2012 Assessingthe complex sponge microbiota core variable and species-specific bacterial com-munities in marine sponges ISME J 6 564ndash576 httpdxdoiorg101038ismej2011116

Schmittner A Oschlies A Matthews HD Galbraith ED 2008 Future changes inclimate ocean circulation ecosystems and biogeochemical cycling simulated for abusiness-as-usual CO2 emission scenario until year 4000 AD Glob BiogeochemCycles 22 GB1013 httpdxdoiorg1010292007gb002953

Schovsbo NH Nielsen AT Klitten K Mathiesen A Rasmussen P 2011 Shale gasinvestigations in Denmark Lower Palaeozoic shales on Bornholm Geol SurvDenmark Greenland Bull 23 9ndash12

Schroumlder S Grotzinger JP 2007 Evidence for anoxia at the EdiacaranndashCambrianboundary the record of redox-sensitive trace elements and rare earth elements inOman J Geol Soc 164 175ndash187 httpdxdoiorg1011440016-76492005-022

Schuster A Erpenbeck D Pisera A Hooper J Bryce M Fromont J Woumlrheide G2015 Deceptive desmas molecular phylogenetics suggests a new classification anduncovers convergent evolution of lithistid demosponges PLoS One 10 e116038httpdxdoiorg101371journalpone0116038

Scrutton CT 1979 Early fossil cnidarians In House MR (Ed) The Origin of MajorInvertebrate Groups Academic London pp 161ndash207

Scrutton CT 1992 Flindersipora bowmani Lafuste and the early evolution of the tabu-late corals Fossil Cnidaria Porifera 21 29ndash33

Scrutton CT 1997 The Palaeozoic corals I origins and relationships Proc Yorks GeolSoc 51 177ndash208 httpdxdoiorg101144pygs513177

Scrutton CT 1999 Palaeozoic corals their evolution and palaeoecology Geol Today15 184ndash193 httpdxdoiorg101046j1365-245119991505005x

Seilacher A 1999 Biomat-related lifestyles in the Precambrian PALAIOS 14 86ndash93httpdxdoiorg1023073515363

Sen Gupta BK Turner RE Rabalais NN 1996 Seasonal oxygen depletion in con-tinental-shelf waters of Louisiana historical record of benthic foraminifers Geology24 227ndash230 httpdxdoiorg1011300091-7613(1996)024lt0227SODICSgt23CO2

Sepkoski Jr JJ 1979 A kinetic model of Phanerozoic taxonomic diversity II EarlyPhanerozoic families and multiple equilibria Paleobiology 5 222ndash251 httpdxdoiorg101017S0094837300006539

Sepkoski Jr JJ 1981 A factor analytic description of the Phanerozoic marine fossil

record Paleobiology 7 36ndash53 httpdxdoiorg101017S0094837300003778Sepkoski Jr JJ 1995 The Ordovician radiations diversification and extinction shown

by global genus-level taxonomic data In Cooper JD Droser ML Finney SC(Eds) Ordovician Odyssey SEPM Pacific section Fullerton CA pp 393ndash396 Specialpublication 77

Servais T Lehnert O Li JUN Mullins GL Munnecke A Nuumltzel A Vecoli M2008 The Ordovician Biodiversification revolution in the oceanic trophic chainLethaia 41 99ndash109 httpdxdoiorg101111j1502-3931200800115x

Servais T Harper DAT Munnecke A Owen AW Sheehan PM 2009Understanding the Great Ordovician Biodiversification Event (GOBE) influences ofpaleogeography paleoclimate or paleoecology GSA Today 19 4ndash10 httpdxdoiorg101130gsatg37a1

Servais T Owen AW Harper DAT Kroumlger B Munnecke A 2010 The GreatOrdovician Biodiversification Event (GOBE) the palaeoecological dimensionPalaeogeogr Palaeoclimatol Palaeoecol 294 99ndash119 httpdxdoiorg101016jpalaeo201005031

Servais T Perrier V Danelian T Klug C Martin R Munnecke A Nowak HNuumltzel A Vandenbroucke TRA Williams M Rasmussen CMOslash 2016 Theonset of the lsquoOrdovician Plankton Revolutionrsquo in the late Cambrian PalaeogeogrPalaeoclimatol Palaeoecol 458 12ndash28 httpdxdoiorg101016jpalaeo201511003

Shapiro RS Rigby JK 2004 First occurrence of an in situ anthaspidellid sponge in adendrolite mound (Upper Cambrian Great Basin USA) J Paleontol 78 645ndash650httpdxdoiorg1016660022-3360(2004)078lt0645FOOAISgt20CO2

Sheehan PM 1985 Reefs are not so differentmdashthey follow the evolutionary pattern oflevel-bottom communities Geology 13 46ndash49 httpdxdoiorg1011300091-7613(1985)13lt46ransdfgt20co2

Shen Y Neuweiler F 2018 Questioning the microbial origin of automicrite inOrdovician calathid-demosponge carbonate mounds Sedimentology 65 303ndash333httpdxdoiorg101111sed12394

Shen Y Zhang T Hoffman PF 2008 On the coevolution of Ediacaran oceans andanimals Proc Natl Acad Sci 105 7376ndash7381 httpdxdoiorg101073pnas0802168105

Shields GA 2017 Earth system transition during the TonianndashCambrian interval ofbiological innovation nutrients climate oxygen and the marine organic carbon ca-pacitor In Brasier AT McIlroy D McLoughlin N (Eds) Earth System Evolutionand Early Life A Celebration of the Work of Martin Brasier Geological Society ofLondon Special Publications Vol 448 pp 161ndash177 httpdxdoiorg101144sp44817

Shields GA Carden GAF Veizer J Meidla T Rong J-Y Li R-Y 2003 Sr C andO isotope geochemistry of Ordovician brachiopods a major isotopic event around theMiddle-Late Ordovician transition Geochim Cosmochim Acta 67 2005ndash2025httpdxdoiorg101016s0016-7037(02)01116-x

Signor PW 1992 Taxonomic diversity and faunal turnover in the early Cambrian didthe most severe mass extinction of the Phanerozoic occur in the Botomian Stage InFifth North American Paleontological Convention Abstracts with Programs 6 pp272

Smith AB 1990 Evolutionary diversification of echinoderms during the earlyPalaeozoic In Taylor PD Larwood GP (Eds) Major Evolutionary RadiationsClarendon Press Oxford pp 265ndash286

Sorauf JE Savarese M 1995 A Lower Cambrian coral from South AustraliaPalaeontology 38 757ndash770

Sperling EA Robinson JM Pisani D Peterson KJ 2010 Wheres the glassBiomarkers molecular clocks and microRNAs suggest a 200-Myr missingPrecambrian fossil record of siliceous sponge spicules Geobiology 8 24ndash36 httpdxdoiorg101111j1472-4669200900225x

Sperling EA Frieder CA Raman AV Girguis PR Levin LA Knoll AH 2013Oxygen ecology and the Cambrian radiation of animals Proc Natl Acad Sci 11013446ndash13451 httpdxdoiorg101073pnas1312778110

Sperling EA Knoll AH Girguis PR 2015a The ecological physiology of Earthssecond oxygen revolution Annu Rev Ecol Evol Syst 46 215ndash235 httpdxdoiorg101146annurev-ecolsys-110512-135808

Sperling EA Wolock CJ Morgan AS Gill BC Kunzmann M Halverson GPMacdonald FA Knoll AH Johnston DT 2015b Statistical analysis of irongeochemical data suggests limited late Proterozoic oxygenation Nature 523451ndash454 httpdxdoiorg101038nature14589

Spincer BR 1996 The palaeoecology of some Upper Cambrian microbial-sponge-eo-crinoid reefs central Texas In Sixth North American Paleontological ConventionAbstracts of Papers pp 367

Stanley GD 2001 The History and Sedimentology of Ancient Reef Systems In Topicsin Geobiology 17 Springer New York (458 pp) httpsdoiorg101007978-1-4615-1219-6

Stearn CW 2015a Functional morphology of the Paleozoic stromatoporoid skeleton InStearn CW (Ed) Treatise on Invertebrate Paleontology Part E Porifera RevisedHypercalcified Porifera Volumes 4 and 5 The University of Kansas PaleontologicalInstitute Lawrence Kansas pp 551ndash573

Stearn CW 2015b Morphologic Affinities of the Paleozoic Stromatoporoidea to otherfossil and recent groups In Stearn CW (Ed) Treatise on Invertebrate PaleontologyPart E Porifera Revised Hypercalcified Porifera Volumes 4 and 5 The University ofKansas Paleontological Institute Lawrence Kansas pp 543ndash549

Steckbauer A Duarte CM Carstensen J Vaquer-Sunyer R Conley DJ 2011Ecosystem impacts of hypoxia thresholds of hypoxia and pathways to recoveryEnviron Res Lett 6 025003 httpdxdoiorg1010881748-932662025003

Stitt JH 1975 Adaptive radiation trilobite paleoecology and extinction PtychaspidBiomere Late Cambrian of Oklahoma In Martinsson A (Ed) Evolution andMorphology of the Trilobita Trilobitoidea and Merostomata Fossils and Strata pp381ndash390

Stolley E 1896 Untersuchungen uumlber coelosphaeridum cyclocrinus mastopora undverwandte genera des silur In Archiu fur Anthropologie und Geologic Schleswig-Holsteins und der benachbarten Gebiete 1 pp 177ndash282 (in German)

Stolper DA Keller CB 2018 A record of deep-ocean dissolved O2 from the oxidationstate of iron in submarine basalts Nature 553 323ndash327 httpdxdoiorg101038nature25009

Strauss H 2006 Anoxia through time In Neretin LN (Ed) Past and Present WaterColumn Anoxia Springer Amsterdam pp 3ndash19 httpdxdoiorg1010071-4020-4297-3_01

Sun N Elias RJ Lee D-J 2014 The biological affinity of Amsassia new evidencefrom the Ordovician of North China Palaeontology 57 1067ndash1089 httpdxdoiorg101111pala12106

Taylor JF 2006 History and status of the biomere concept Mem Assoc AustrPalaeontol 32 247ndash265

Taylor MW Radax R Steger D Wagner M 2007 Sponge-associated microorgan-isms evolution ecology and biotechnological potential Microbiol Mol Biol Rev71 295ndash347 httpdxdoiorg101128MMBR00040-06

Taylor JF Repetski JE Loch JD Leslie SA 2012 Biostratigraphy and chronos-tratigraphy of the CambrianndashOrdovician Great American Carbonate Bank In DerbyJR Fritz RD Longacre SA Morgan WA Sternbach CA (Eds) The GreatAmerican Carbonate Bank The Geology and Economic Resources of the Cambrian-Ordovician Sauk Megasequence of Laurentia AAPG Memoir 98 AAPG pp 15ndash35httpdxdoiorg10130613331488M983497

Taylor PD Berning B Wilson MA 2013 Reinterpretation of the Cambrian lsquobryozoanPywackia as an octocoral J Paleontol 87 984ndash990 httpdxdoiorg10166613-029

Teslenko IL Mambetov AM Zhuravleva IT Myagkova YI Meshkova NP 1983The Dedebulak bioherm belt and the history of its development Trudy InstitutaGeologii i Geofiziki Sibirskoye Otdeleniye 569 124ndash138 (in Russian)

Thomas TR Kavlekar DP LokaBharathi PA 2010 Marine drugs from sponge-mi-crobe association-a review Marine Drugs 8 1417ndash1468 httpdxdoiorg103390md8041417

Thompson CK Kah LC 2012 Sulfur isotope evidence for widespread euxinia and afluctuating oxycline in Early to Middle Ordovician greenhouse oceans PalaeogeogrPalaeoclimatol Palaeoecol 313-314 189ndash214 httpdxdoiorg101016jpalaeo201110020

Thompson CK Kah LC Astini R Bowring SA Buchwaldt R 2012 Bentonitegeochronology marine geochemistry and the Great Ordovician BiodiversificationEvent (GOBE) Palaeogeogr Palaeoclimatol Palaeoecol 321-322 88ndash101 httpdxdoiorg101016jpalaeo201201022

Toomey DF 1970 An unhurried look at a Lower Ordovician mound horizon southernFranklin Mountains west Texas J Sediment Petrol 40 1318ndash1334 httpdxdoiorg10130674D72194-2B21-11D7-8648000102C1865D

Toomey DF Ham WE 1967 Pulchrilamina a new mound-building organism fromLower Ordovician rocks of west Texas and southern Oklahoma J Paleontol 41981ndash987

Toomey DF Nitecki MH 1979 Organic buildups in the Lower Ordovician (Canadian)of Texas and Oklahoma In Fieldiana Geology 2 History Field Museum of Natural(181 pp)

Tripathy GR Hannah JL Stein HJ Yang G 2014 Re-Os age and depositionalenvironment for black shales from the Cambrian-Ordovician boundary Green Pointwestern Newfoundland Geochem Geophys Geosyst 15 1021ndash1037 httpdxdoiorg101002

Trotter JA Williams IS Barnes CR Lecuyer C Nicoll RS 2008 Did coolingoceans trigger Ordovician biodiversification Evidence from conodont thermometryScience 321 550ndash554 httpdxdoiorg101126science1155814

Tunnicliffe V 1981 High species diversity and abundance of the epibenthic communityin an oxygen-deficient basin Nature 294 354ndash356 httpdxdoiorg101038294354a0

Tyson RV Pearson TH 1991 Modern and ancient continental shelf anoxia anoverview In Tyson RV Pearson TH (Eds) Modern and Ancient ContinentalShelf Anoxia Geological Society of London Special Publications 58 GeologicalSociety of London London pp 1ndash24 httpdxdoiorg101144GSLSP19910580101

Van Iten H Marques AC Leme JdM Pacheco MLAF Simotildees MG Smith A2014 Origin and early diversification of the phylum Cnidaria Verrill major devel-opments in the analysis of the taxons Proterozoic-Cambrian history Palaeontology57 677ndash690 httpdxdoiorg101111pala12116

Van Roy P Orr PJ Botting JP Muir LA Vinther J Lefebvre B el Hariri KBriggs DE 2010 Ordovician faunas of Burgess Shale type Nature 465 215ndash218httpdxdoiorg101038nature09038

Vinn O Zatoń M 2012 Inconsistencies in proposed annelid affinities of early biomi-neralized organism Cloudina (Ediacaran) structural and ontogenetic evidences InNotebooks on Geology CG2012_A03 pp 39ndash47

Vologdin AG 1961 Archaeocyaths and their stratigraphic significance InternationalGeological Congress XX Session Mexico The Cambrian System its Paleogeographyand Lower Boundary Problem Volume 3 Western Europe Africa USSR AsiaAmerica Akademiya Nauk SSSR Moscow pp 173ndash199

Vologdin AG Zhuravleva IT 1947 Morphology of regular archaeocyaths Abstracts ofScientific Research for 1945 Academy of Sciences of the USSR Division of BiologicalSciences Moscow and Leningrad pp 227ndash228

Wallace MW Hood Av Shuster A Greig A Planavsky NJ Reed CP 2017Oxygenation history of the Neoproterozoic to early Phanerozoic and the rise of landplants Earth Planet Sci Lett 466 12ndash19 httpdxdoiorg101016jepsl201702046

Webb GE 1999 Youngest Early Carboniferous (late Visean) shallow-water patch reefsin eastern Australia (Rockhampton Group Queensland) combining quantitativemicro- and macro-scale data Facies 41 111ndash140 httpdxdoiorg101007BF02537462

Webby BD 2002 Patterns of Ordovician reef development In Kiessling W Fluumlgel EGolonka J (Eds) Phanerozoic Reef Patterns SEPM Special Publication 72 SEPMTulsa pp 129ndash179 httpdxdoiorg102110pec02720129

Webby BD 2015 Class uncertain order Pulchrilaminida new order In Stearn CW

(Ed) Treatise on Invertebrate Paleontology Part E Porifera Revised HypercalcifiedPorifera Volumes 4 and 5 The University of Kansas Paleontological InstituteLawrence Kansas pp 837ndash844

Webby BD Paris F Droser ML Percival IG 2004 The Great OrdovicianBiodiversification Event Columbia University Press New York (497 pp)

Werner W Leinfelder RR Fuumlrsich FT Krautter M 1994 Comparative palaeoe-cology of marly coralline sponge-bearing reefal associations from the Kimmeridgian(Upper Jurassic) of Portugal and southwestern Germany Courier ForschungsinstitutSenckenberg 172 381ndash397

West RR 2012 Evolution of the hypercalcified chaetetid-type porifera (Demospongiae)In Stearn CW (Ed) Treatise on Invertebrate Paleontology Part E PoriferaRevised Hypercalcified Porifera Volumes 4 and 5 The University of KansasPaleontological Institute pp 1ndash26

Westrop SR Ludvigsen R 1987 Biogeographic control of trilobite mass extinction atan Upper Cambrian biomere boundary Paleobiology 13 84ndash99 httpdxdoiorg101017S0094837300008605

Wilde P Berry WBN 1984 Destabilization of the oceanic density structure and itssignificance to marine extinction events Palaeogeogr Palaeoclimatol Palaeoecol48 143ndash162 httpdxdoiorg1010160031-0182(84)90041-5

Wilde P Quinby-Hunt MS Berry WBN Orth CJ 1989 Palaeo-oceanography andbiogeography in the Tremadoc (Ordovician) Iapetus Ocean and the origin of thechemostratigraphy of Dictyonema flabelliforme black shales Geol Mag 126 19ndash27httpdxdoiorg101017s0016756800006117

Williams M Vannier J Corbari L Massabuau JC 2011 Oxygen as a driver of earlyarthropod micro-benthos evolution PLoS One 6 e28183 httpdxdoiorg101371journalpone0028183

Woo J 2009 The Middle Cambrian Zhangxia Formation Shandong Province Chinadepositional environments and microbial sedimentation Seoul National UniversitySeoul (243 pp PhD Thesis)

Wood R 1999 Reef Evolution Oxford University Press Oxford (414 pp)Wood R 2017 Palaeoecology of Ediacaran metazoan reefs In Brasier AT McIlroy D

McLoughlin N (Eds) Earth System Evolution and Early Life A Celebration of theWork of Martin Brasier Geological Society of London Special Publications Vol 448pp 195ndash210 httpdxdoiorg101144sp4481

Wood R Erwin DH 2018 Innovation not recovery dynamic redox promotes me-tazoan radiations Biol Rev 93 863ndash873 httpsdoiorg101111brv12375

Wood RA Evans KR Zhuravlev AY 1992 A new post-early Cambrian archaeocyathfrom Antarctica Geol Mag 129 491ndash495 httpdxdoiorg101017S0016756800019579

Wood R Zhuravlev AY Anaaz CT 1993 The ecology of Lower Cambrian buildupsfrom Zuune Arts Mongolia implications for early metazoan reef evolutionSedimentology 40 829ndash858 httpdxdoiorg101111j1365-30911993tb01364x

Wood RA Grotzinger JP Dickson JAD 2002 Proterozoic modular biomineralizedmetazoan from the Nama Group Namibia Science 296 2383ndash2386 httpdxdoiorg101126science1071599

Wood RA Poulton SW Prave AR Hoffmann KH Clarkson MO Guilbaud RLyne JW Tostevin R Bowyer F Penny AM Curtis A Kasemann SA 2015Dynamic redox conditions control late Ediacaran metazoan ecosystems in the NamaGroup Namibia Precambrian Res 261 252ndash271 httpdxdoiorg101016jprecamres201502004

Wrona R Zhuravlev AY 1996 Early Cambrian archaeocyaths from glacial erratics ofKing George Island (South Shetland Islands) Antarctica Palaeontol Pol 55 10ndash36

Xiao S 2014 Evolution the making of Ediacaran giants Curr Biol 24 R120ndashR122httpdxdoiorg101016jcub201312035

Yin Z Zhu M Davidson EH Bottjer DJ Zhao F Tafforeau P 2015 Sponge gradebody fossil with cellular resolution dating 60Myr before the Cambrian Proc NatlAcad Sci 112 E1453ndashE1460 httpdxdoiorg101073pnas1414577112

Young SA Gill BC Edwards CT Saltzman MR Leslie SA 2016 MiddlendashLateOrdovician (DarriwilianndashSandbian) decoupling of global sulfur and carbon cyclesisotopic evidence from eastern and southern Laurentia Palaeogeogr PalaeoclimatolPalaeoecol 458 118ndash132 httpdxdoiorg101016jpalaeo201509040

Yu B Dong H Widom E Chen J Lin C 2009 Geochemistry of basal Cambrianblack shales and cherts from the Northern Tarim Basin Northwest China implica-tions for depositional setting and tectonic history J Asian Earth Sci 34 418ndash436httpdxdoiorg101016jjseaes200807003

Zamora S Clausen S Alvaro JJ Smith AB 2010 Pelmatozoan echinoderms ascolonizers of carbonate firmgrounds in mid-Cambrian high energy environmentsPALAIOS 25 764ndash768 httpdxdoiorg102110palo2010p10-052r

Zamora S Lefebvre B Javier Alvaro J Clausen S Elicki O Fatka O Jell PKouchinsky A Lin JP Nardin E Parsley R Rozhnov S Sprinkle J SumrallCD Vizcaino D Smith AB 2013 Cambrian echinoderm diversity and palaeo-biogeography In Harper DAT Servais T (Eds) Early Palaeozoic Biogeographyand Palaeogeography Geological Society London Memoirs 1 The GeologicalSociety of London London pp 157ndash171 httpdxdoiorg101144m3813

Zamora S Deline B Javier Aacutelvaro J Rahman IA 2017 The Cambrian SubstrateRevolution and the early evolution of attachment in suspension-feeding echinodermsEarth Sci Rev 171 478ndash491 httpdxdoiorg101016jearscirev201706018

Zhang X Shu D Han J Zhang Z Liu J Fu D 2014 Triggers for the Cambrianexplosion hypotheses and problems Gondwana Res 25 896ndash909 httpdxdoiorg101016jgr201306001

Zhang L Chang S Khan MZ Feng Q Danelian T Clausen S Tribovillard NSteiner M 2018 The link between metazoan diversity and paleo-oxygenation in theearly Cambrian an integrated palaeontological and geochemical record from theeastern three gorges region of South China Palaeogeogr Palaeoclimatol Palaeoecol495 24ndash41 httpdxdoiorg101016jpalaeo201712007

Zhu M Babcock L Peng S 2006 Advances in Cambrian stratigraphy and pa-leontology integrating correlation techniques paleobiology taphonomy and pa-leoenvironmental reconstruction Palaeoworld 15 217ndash222 httpdxdoiorg101016jpalwor200610016

Zhuravlev AY 1996 Reef ecosystem recovery after the Early Cambrian extinction InHart MB (Ed) Biotic Recovery from Mass Extinction Events Geological Society ofLondon Special Publications 102 Geological Society of London Oxford pp 79ndash96httpdxdoiorg101144GSLSP19960010106

Zhuravlev AY 1999 А new coral from the Lower Cambrian of Siberia Paleontol Zh 527ndash33 (in Russian with English abstract)

Zhuravlev AY 2001a Biotic diversity and structure during the Neoproterozoic-Ordovician transition In Zhuravlev AY Riding R (Eds) Ecology of the CambrianRadiation Columbia University Press New York pp 173ndash199

Zhuravlev AY 2001b Paleoecology of Cambrian reef ecosystems In Stanley GD(Ed) The History and Sedimentology of Ancient Reef Systems Kluwer AcademicPlenum Publishers New York pp 121ndash157 httpdxdoiorg101007978-1-4615-1219-6_4

Zhuravlev AY Wood R 1995 Lower Cambrian reefal cryptic communitiesPalaeontology 38 443ndash470

Zhuravlev AY Wood RA 1996 Anoxia as the cause of the mid-Early Cambrian(Botomian) extinction event Geology 24 311ndash314 httpdxdoiorg1011300091-7613(1996)024lt0311aatcotgt23co2

Zhuravlev AY Debrenne F Lafuste J 1993 Early Cambrian microstructural di-versification of Cnidaria Courier Forschungsinstitut Senckenberg 164 365ndash372

Zhuravlev AY Naimark EB Wood RA 2015 Controls on the diversity and structureof earliest metazoan communities early Cambrian reefs from Siberia Earth Sci Rev147 18ndash29 httpdxdoiorg101016jearscirev201504008

Zhuravleva IT Myagkova EI 1987 Primitive phanerozoic multicellular organisms InInstitute of Geology and Geophysics Siberian Branch Academy of Sciences of theUSSR Transactions 695 Nauka Moscow (224 pp)

Marine oxygenation lithistid sponges and the early history of Paleozoic skeletal reefs

Introduction

CambrianndashOrdovician marine diversity

Late Ediacaranndashmid-Ordovician eukaryote reef development

Late Ediacaran (~550ndash541 Ma) microbial-Cloudina

Earliest Cambrian Fortunianmid-Age 2 (541ndash525 Ma) microbial-ldquoLadathecardquo

Early Cambrian mid-Age 2late Age 4 (525ndash510 Ma) microbial-archaeocyath

Archaeocyaths

Cribricyaths radiocyaths

Early Cambrian coralomorphs

Chaetetids

Pelmatozoans

Midndashlate Cambrian (ldquoreef gaprdquo) late Age 4end Age 10 (510ndash485 Ma) microbial-lithistid

EarlyndashMiddle Ordovician (485ndash460 Ma) microbial-lithistid-calathiid-pulchrilaminid

Receptaculitids radiocyaths cyclocrinitids

Bryozoans

Pulchrilaminids

Corals

Late MiddlendashLate Ordovician (460ndash444 Ma) stromatoporoid-bryozoan-tabulate-receptaculitid-microbial

Midndashlate Cambrian lithistid sponge-microbial reefs

Zhangxia Formation (upper Stage 5 Cambrian Series 3) Shandong China

Ranken Limestone (upper Drumian Cambrian Series 3) Georgina Basin Australia

Deh-Molla Formation (lower Paibian Furongian) northern Iran

Notch Peak Formation (Stage 10 Furongian) Nevada USA

Summary

Midndashlate Cambrian dysoxia-hypoxia and sponge-microbial reefs

Evidence for low-oxygen conditions

Factors promoting low-oxygen conditions in shallow marine environments

Low oxygen levels and lithistid sponges

Mid-Cambrian to Early Ordovician reef development

Overview

Conclusions

Acknowledgements

Supplementary data

References